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Volume 28 Evolution
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Preface
Volume 24 2.
Pages xi-xiii
pp. 1-480 (2005)
Behaviour and Physiology of Fish Barbara A. Block, E. Donald Stevens
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Fish Biomechanics
Volume 22 Systematics of the tunas and mackerels
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(Scombridae)
Physiology of Polar Fishes
Pages 1-33
Volume 21 Bruce B. Collette, Carol Reeb, Barbara A.
pp. 1-634 (2005) Block
The Physiology of Tropical Fishes
Nitrogen Excretion
Volume 19 Tuna metabolism and energetics
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Tuna: Physiology, Ecology, and
Evolution Keith E. Korsmeyer, Heidi Dewar
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Molecular Endocrinology of Fish
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The Cardiovascular System Advances in acoustic, archival, and
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Volume 12, Part 1 satellite tagging of tunas
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The Cardiovascular System John Gunn, Barbara Block
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Viviparity and Posthatching Juveniles
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Acid-Base Regulation
Mark W. Westneat, Stephen A. Wainwright
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Reproduction and Growth 13.
Bioluminescence, Pigments, and Pages 413-459
Poisons Carl Safina
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The Endocrine System
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CONTRIBUTORS
The numbers in parentheses indicate the pages on which the authors’ contributions begin
JOHN ALTRINGHAM (313), School of Biology, University of Leeds, Leeds LS2 957:
United Kingdom
BARBARA BLOCK (1, 167), Hopkins Marine Station, Stanford University, Pacific
Grove, California 93950
RICHARD BRILL (79), National Marine Fisheries Service, Southwest Fisheries Sci-
ence Center, Honolulu Laboratory, Honolulu, Hawaii 96822-2396
PETER BUSHNELL (79), Department of Biological Sciences, Indiana University
South Bend, South Bend, Indiana 46634-71 I1
BRUCE COLLETTE (I), NMFS Systematics Lab, National Museum of Natural His-
tory, Washington, DC 20560-0153
HEIDI DEWAR (35), Pfleger Institute of Environmental Research, Oceanside, Cal-
ifornia 92054
KATHRYN DICKSON (1219, Department of Biological Science, Caltfornia State
University Fullerton, Fullerton California 92834
CHARLES A. FARWELL (3911, Monterey Bay Aquarium, Monterey, California

93940
JEFFREY GRAHAM (121), Center for Marine Biotechnology and Biomedicine,
Scripps Institute of Oceanography, University of Caltfomia at San Diego, La
Jolla, California 92093-02045
JOHN S. GUNN (167), CSIRO Marine Research, Hobart, Australia 7000
KEITH KORSMEYER (3.5), Hawaii Puc$ic University, Kaneohe, Hawaii 96744
CAROL REEB (11, Hopkins Marine Station, Stanford University, Pacijc Grove,
California 93950
ix
X CONTRIBUTORS
CARL SAFINA (413), Living Oceans Program, National Audubon Society, Islip,
New York 117.51
ROBERTSHADWICK(313), Marine Biology Research Division, Scripps Institute of
Oceanography, University of California at San Diego, La Jolla, California
92093
KURT SCHAEFER(225) Inter-American Tropical Tuna Commission, La Jolla,
California 92093
GARY SHARP(34.5) Center for Climate/Ocean Resources Study, Monterey, Cali-
fornia 93940
STEPHENWAINWRIGHT(271), Department of Zoology, Duke University, Durham,
North Carolina 27706
MARK WESTNEAT(271), Department of Zoology, Field Museum of Natural His-
tory, Chicago, Illinois 606052496
PREFACE
Watching a tuna swim, you can’t help but be impressed by its power, grace,
and speed. If you’ve tried to catch a tuna on a fishing line, you have undoubtedly
discovered its tremendous strength. Its superbly streamlined shape reflects its
ceaseless activity. Even the scientific family name of the tunas, Thunnlas, comes
from the Greek verb thuno-meaning rush. Almost 40 years ago the real life of
tunas was hinted at when a bluefin tuna tagged in the Bahamas was caught less
than 50 days later off the coast of Norway, 6700 km distant (Mather, 1962). This
migratory lifestyle and the extraordinary anatomical and physiological features
that permit it have interested observers since Aristotle. Hunting, catching, and
even the study of tunas have long been intertwined with ancient cultures and tradi-
tions (Maggio, 2000). Over the past two decades, tuna science has sparked new
interest and the participation of a large number of very talented biologists using
innovative techniques.
Tunas are, of course, very valuable and this has raised interest in the fish as
a commodity. Although they constitute less than 5% of the world’s commercial
catch by weight, they contribute a much larger fraction by dollar value. Bluefin
tunas are among the most valuable fish in the sea. Nearly every year since the mid-
1970s another fish has been ‘awarded’ a new highest-ever price, $10,000,
$12,000 . . . to upward of $35,000. In January 2001 an individual fish sold for
$175,000 in Tokyo. This value has created huge incentive for those trying to catch
tunas for profit. It has also sparked concern and passion among those trying to
prevent bluefin tuna from being fished to extinction.
This volume reflects the growing interests of two types of researchers that
study tuna: one driven by the discovery of the extraordinary morphological and
physiological features that make tuna unique, and the other by fisheries’ concerns.
Our book is an attempt to synthesize and integrate both basic and applied research
within one volume. We examine the relationships of tunas, mackerels, and boni-
tos; their evolutionary history; the recent technological advances in our knowl-
edge of their metabolism, cardiovascular physiology, and reproductive biology;
and the physiological ecology and oceanography of tunas in the oceans.
The unique features of the circulatory systems and internalization of the
slow-oxidative swimming muscles of the tunas prompted Kishinouye (1923) to
ui
xii PREFACE
place tunas in their own order, the Plecostei, to separate them from all other te-
leosts. This suggestion was not generally accepted by systematists, but highlights
the uniqueness that many early researchers noted. The chapter by Collette, Reeb,
and Block shows us that the systematics of tunas and their relatives is controversial
and requires further study.
Despite the practical challenges of working with tunas that limit rapid ad-
vances in studies of tuna physiology and morphology, this volume demonstrates
that significant findings have emerged from the past two decades of laboratory and
field research. Tunas have exceptional cardiac performance, high metabolic rates,
and endothermic traits. Tunas utilize metabolic heat to warm the muscle, viscera,
brain, and eyes, but the heart operates at ambient water temperatures. Just to
supply oxygen to the tuna’s endothermic swimming muscles requires an extraor-
dinary metabolism and a unique cardiac system when compared to all other te-
leosts. Korsmeyer and Dewar summarize information on metabolism and aerobic
capacity of tunas, and Brill and Bushnell focus on the cardiovascular and respira-
tory features required to acquire and deliver oxygen to the tissues. Graham and
Dickson review the recent laboratory studies on the thermoregulation of tunas and
examine morphological and physiological traits associated with endothermy in a
phylogenetic context. Westneat and Wainwright use gross dissection of tunas and
their relatives to provide information on the linkages between tendon, muscle, and
bone that make tunas efficient swimmers. This chapter is complemented by a
chapter on physiology of the swimmers muscles by Altringham and Shadwick.
They apply modern techniques of muscle physiology of hydrodynamical analysis
to tuna swimming and show the mechanical advantage of warm muscles. In ad-
dition, they provide an analysis of the characteristic swimming form of the group:
thunniform swimming.
The chapter by Schaefer is a fascinating account of the reproductive lifestyle
and its huge annual metabolic cost in tunas. All tunas are oviparous, multiple
spawners and shed their gametes directly into the sea at locales where sea-surface
temperatures are warm. For some species such as the giant bluefins, this brief
period in warm waters may be the most physiologically demanding. The chapter
by Sharp shows that considerable insight into tuna lifestyles has been achieved by
looking when, where, and how commercial fishers seek and catch them. We learn
that tuna are constrained to some extent by the availability of oxygen and appro-
priate water temperatures and that these constraints depend on time of day, season,
stage of development, and reproductive status. The tuna lifestyle seems to have
three phases: feeding, traveling, and reproduction. Technology has had the great-
est impact in revealing details about the lifestyle of tunas. The major breakthrough
is the development of devices that can record and archive data so that it is no
longer essential to follow a fish with a ship. We knew tuna had a capacity for huge
migrations, but little was known about the day-to-day life of a tuna. The chapter
by Gunn and Block reveals much in this regard. Conventional tag data yielded
. ..
PREFACE x111
two data points (release and capture location). Modern tags can reveal depth, ex-
ternal and internal temperature every few minutes, and daily locations yielding
tens of thousands of data points. Before there was a paucity; now we may be
overwhelmed by the volume of data. Over 20,000 days of archival data have been
collected in the past five years and knowledge of what tunas really do is becoming
a reality.
By increasing knowledge about tunas we can hope to ensure their future on
Earth. This book appears at a time when it is more vital than ever to begin to close
the gap between what we know about tunas and what we need to know. Tunas are
apex pelagic predators who are threatened by little except expansion of our own
species. As Carl Safina eloquently writes in his chapter, “Can tunas bear the ap-
petite of a world with 6 billion people?” Tunas are increasingly being retained in
pens for growout, study, and display, as Farwell describes in his chapter, “Tunas
in Captivity.” Scientists and “ranchers” alike seek to raise tunas through their life
cycle for knowledge as well as profit.
We express our sincerest thanks to the authors for their contributions and to
the reviewers who enriched their content. The Block and Stevens labs helped
throughout the process and we thank our students for their contributions. We dedi-
cate our book to the two Franks: Carey and Mather. Frank Carey inspired many
of us to think more about how and why tunas stay warm and pioneered the study
of tunas in the wild. Frank Mather spent a lifetime trying to figure out the puzzle,
which remains unsolved to this day, of the movements of the most noble fish in
the sea, the Atlantic bluefin tuna. They shared their enthusiasm for tuna and the
sea first with one another, and then just as enthusiastically with us. We hope this
volume reflects their spirit and commitment to tuna biology and scientific
excellence.
Barbara A. Block
E. Donald Stevens
Kishinouye, K. (1923). Contributions to the comparative study of the so-called scombroid fishes.
J. Coil. Agric. Imp. Univ. Tokyo 8, 293-475.
Maggio, T. (2001). Maffanza. The Ancient Sicilian Ritual of Bluefin Tuna Fishing. Penguin. New
York.
Matber, F. (1962). Transatlantic migration of two large bluefin tuna. J. Conseil Penn. hr. Exploration
Mer. 27. 325-327.
1
SYSTEMATICS OF THE TUNAS AND MACKERELS

(SCOMBRIDAE)
BRUCE B. COLLETTE
CAROL REEB
BARBARA A. BLOCK
1. Morphological Systematics
A. Gasterochismatinae Lahille, 1903
B. Subfamily Scombrinae Bonaparte, 183 1
II. Molecular Systematic5
A. Are Billfishes Scombroid Fishes?
B. Is Gasterochismatinae a Sister Group to the Scombrinae’?
C. Can Molecular Phylogenies Resolve the Thunnini and Sardini Tribes’?
D. Problems Caused by Partial Sequences and Homoplasy
E. Are Thunnus Monophyletic?
F. Has Mitochondrial Introgression Occurred between Bluetin and Albacore Tuna?
G. Can Molecular Data Resolve the Relationships among Spanish Mackerels?
H. Is Scomber scombrus Generically Different from Scomberjaponicus and Scornher
australasicus?
III. Conclusions
The Scombridae is a family of 1.5 genera and about 50 species of epipelagic

marine fishes (see Table I). They possess many morphological and physiological
adaptations that are of great interest to physiologists and evolutionary biologists.
Mackerels, Spanish mackerels, bonitos, and tunas form the basis of important
commercial and recreational fisheries throughout tropical and temperate waters of
the world.
The currently accepted classification (Collette and Nauen, 1983; Collette
et al., 1984) of the mackerels and tunas (family Scombridae) within the suborder
Scombroidei (Figure 1) is largely based on classical morphological studies of
Kishinouye (1923), Godsil and co-workers (e.g., Godsil and Byers, 1944; Godsil,
1954), and Johnson (1986), and research by Collette with a series of co-workers
I
Turn Volume 19 Copyright 0 2001 by Academic Press
FISH PHYSIOLOGY All rights of reproduction m any form reserved.
BRUCE B. COLLETTE ET AL
Table 1
Synopsis of Scombrid Classification
Subfamily Gasterochismatinae Labille, 1903

Gasterochisma Richardson, 1845
Gasterochisma melampus Richardson, 1845
Subfamily Scombrinae Bonaparte, 183 1
Tribe Scombrini Bonaparte, 183 1
Rasfrelliger Jordan and Starks, 1908
RastrelIiger brachysoma (Bleeker, 185 1)
Rastrelligerfaughni Matsui, 1967
Rastrelliger kunagurta (Cuvier, 18 16)
Scomber Linnaeus, 1758
Scomber australasicus Cuvier in Cuvier and Valenciennes, 1832
Scomberjaponicus Houttuyn, 1782
Scomber colias Gmelin, 1789
Scomber scombrus Linnaeus, 1758
Tribe Scomberomorini Starks, 19 IO
Acanthocybium Gill, 1862
Acanthocybium solandri (Cuvier in Cuvier and Valenciennes, 1832)
Grammatorcynus Gill, 1862
Grammatorcynus bicarinatus (Quoy and Gaimard, 1825)
Grammatorcynus bilineatus (Rtippell, 1836)
Scomberomorus Lacepede, 180 1
Scomberomorus brasilensis Collette, Russo, and ZavaJa-Camin, 1978
Scomberomorus cavalla (Cuvier, 1829)
Scomberomorus commerson (Lacepede, 1800)
Scomberomorus concolor (Lockington, 1879)
Scomberomorus guttatus (Bloch and Schneider, 1801)
Scomberomorus koreanus (Kishinouye, 1915)
Scomberomorus Zineolatus (Cuvier in Cuvier and Valenciennes, 183 1)
Scomberomorus maculatus (Mitchill, 1815)
Scomberomorus mulfiradiatus Munro, 1964
Scomberomorus munroi Collette and Russo, 1980
Scomberomorus niphonius (Cuvier in Cuvier and Valenciennes, 1832)
Scomberomorus plurilineatus Fourmanoir, 1966
Scomberonwrus queenslandicus Munro, 1943
Scomberomorus regalis (Bloch, 1793)
Scomberomorus semifasciafus (Macleay, 1883)
Scomberomorus sierra Jordan and Starks in Jordan, 1895
Scomberomorus sinensis (Lacep&de, 1800)
Scomberonwrus triter (Cuvier in Cuvier and Valenciennes, 1832)
Tribe Sardini Jordan and Evermann, 1896
Cybiosarda Whitley, 1935
Cybiosarda elegans (Whitley, 1935)
Gymnosarda Gill, 1862
Gymnosarda unicolor (Rtippell, 1836)
Orcynopsis Gill, 1862
Orcynopsis unicolor (E. Geoffroy St. Hilaire, 18 17)
1. SYSTEMATICS OF THE TUNAS AND MACKERELS
Sat& Cuvier, 1829

Sarda ausrrulis (Macleay, 188 1)
Sarda chiliensis chiliensis (Cuvier in Cuvier and Valenciennes, 1832)
Sarda chiliensis lineolata Girard. 1859
Sarda orientalis (Temminck and Schlegel, 1844)
Sardu surdu (Bloch, 1793)
Tribe Thunnini Starks, 19 IO
Allothumus Serventy, 1948
Allothunnusfallai Serventy, 1948
Amis Cuvier, 1829
Amis Cuvier, 1829
Au.xis rochei rochei (R&o, 1810)
Auxis rochei eudoran Collette and Aadland, 1996
Auxis thazard thazard (Lacepede, 1800)
Auk thazard brachydorax Collette and Aadland, 1996
Euthynnus Ltitken, 1882
Euthynnus afinis (Cantor, 1849)
Euthynnus af1etteratu.s (Rafinesque, I8 10)
Euthynnus linearus Kishinouye, 1920
Katsuwonus Kishinouye, 1923
Katsuwonuspelamis (Linnaeus. 1758)
Thunnus South, I845
(Thunnus South, 184.5)
Thunnus aialunga (Bonnaterre, 1788)
Thunnus maccoyii (Castlenau, 1872)
Thunnus obesus (Lowe, 1839)
Thunnus thynnus (Linnaeus, 1758)
Thunnus orient&r (Temminck and Schlegel. 1844)
(Neothunnu Kishinouye, 1923)
Thunnus albacures (Bonnaterre, 1788)
Thunnus atlanticus (Lesson, 183 I )
Thunnus tonggo (Bleeker, 1851)
starting in the 1960s (e.g., Gibbs and Collette, 1967; Collette and Chao, 1975;
Collette and Russo, 1985b; Carpenter et al., 1995; Collette and Gillis, 1992; Col-
lette and Aadland, 1996; Collette, 1999). Recently, a number of investigators have
begun to test portions of this classification with molecular methods using both
nuclear and mitochondrial DNA (mtDNA), raising some taxonomic questions
and controversies (Bartlett and Davidson, 1991; Block et al., 1993; Finnerty and
Block, 1995; Chow and Kishino, 1995; Elliot and Ward, 1995; Alvarado Bremer
et al., 1996). This chapter presents a synopsis of scombrid systematics based on
classical morphological characters followed by an examination of some of these
hypothesized relationships using genetic data. In the future a combination of
molecules and morphology should provide the best approximation of relation-
ships among scombrids.
4 BRUCE B. COLLETTE ETAL
Thunnus
Katsuwonus
Euthynnus
THUNNINI
Auxis
Allothunnus
Sarda
SARDINI Gymnosarda
Cybiosarda
Orcynopsis
Grammatorcynus
SCOMBRINAE SCOMBEROMORINI
Acanthocybium
Scomberomorus
SCOMBRINI I Rastrelliger
2 Scomber
GASTEROCHISMATINAE
Gasterochisma
Fig. 1. Morphological tree of the family Scombridae (from Collette and Russo, 1985a), with
permission.
1. SYSTEMATICSOFTHETUNAS ANDMACKERELS
I. MORPHOLOGICAL SYSTEMATICS
A. Gasterochismatinae Lahille. 1903
1. GASTEROCHISMA RICHARDSON, I 845

This distinctive monotypic genus is of a different and more primitive evolu-
tionary lineage than the other scombrids. Gasterochisma melampus Richardson,
1845, appears different enough morphologically from other scombrids that it may
well belong in a separate family. It has very large cycloid scales and two anterior
projections of the swim bladder that extend into the back of the skull, close to the
inner ear. The pelvic fins are huge in juveniles but become proportionally smaller
as the fish increases in size. At all sizes the pelvic fins fit into a groove much as
the first dorsal spines do in all scombrids. There is a thick layer of fat under the
scales, perhaps an adaptation to the cold waters of its habitat around the world at
low latitudes of the Southern Ocean. It has a brain heater derived from the lateral
extraocular muscle, which is distinct in its muscular origin from the heater organ
of the billfishes (Block, 1994). Gasterochisma lacks the median keel on the caudal
peduncle and has only the pair of small keels on each side of the base of the caudal
fin that are characteristic of all scombrids. Gasterochisma reaches a large size (over
1320 mm fork length). The number of vertebrae are 21 precaudal plus 23 caudal.
B. Subfamily Scombrinae Bonaparte, 183 1
The subfamily Scombrinae is composed of two groups of two tribes. The more
primitive mackerels (Scombrini) and Spanish mackerels (Scomberomorini) have
a distinct notch in the hypural plate, lack any bony support for the median fleshy
caudal peduncle keels, and do not have the penultimate vertebral centra greatly
shortened.
1. TRIBESCOMBRINIBONAPARTE, 1831
Two genera of mackerels have been recognized, Scomber and Rastrelliger,
each with three species (Matsui, 1967). Mackerels have small conical teeth and
many gill rakers. They have the fewest vertebrae (31) in the family and only two
small caudal peduncle keels, lacking the median keel found in higher scombrids.
Scomber and Rastrelliger differ in a number of anatomical characters (Matsui,
1967). For Scomber, these characters include the following: teeth present on the
vomer and palatines, last branchiostegal ray only slightly flattened, 12-28 inter-
neural bones under first dorsal fin, first haemal spine somewhat flattened and bent
backward (Matsui, 1967, Figure 4), first interhaemal bone anterior to haemal spine
of 15th vertebra, and finally, vertebrae 3 1 and either 13 or 14 being precaudal
while vertebrae 17 or 18 are caudal.
6 BRUCE B. COLLETTE ETAL.
Matsui (1967) recognized three species of Scomber: S. scombrus Linnaeus,

1758; S. australasicus Cuvier, 1832; and S. japonicus Houttuyn, 1782, a polytypic
worldwide antitropical species. The species differ in a series of characters sum-
marized by Matsui (1967, Table 5). These characters include the sculpturing of
the skull, number of precaudal vertebrae (13 in S. scombrus; 14 in the other two
species), arrangement of palatine teeth, number of interneural bones under the first
dorsal fin (12-15 in S. japonicus, 15-20 in S. austrdasicus, and 21-28 in S.
scombrus), number of first dorsal spines, relative length of space between dorsal
fins, presence of swim bladder (absent only in S. scombrus), and color pattern.
Scomber scombrus is restricted to the North Atlantic, with populations in both
the western and the eastern North Atlantic. Scomber australasicus has been con-
sidered to be restricted to the Pacific Ocean and southeast Indian Ocean, with
major populations in the northwestern Pacific-Japan, Taiwan, and Philippines-
the southwestern Pacific, Australia, and New Zealand, plus a small population in
the Revillagigedo Islands off the coast of Mexico in the eastern Pacific. However,
more recently, it has been found to occur in the northern Indian Ocean and Red
Sea (Baker and Collette, 1998).
Scomber japonicus has been considered to be the most widespread species in
the genus, sympatric with S. scombrus in the North Atlantic and with S. austra-
Zasicusin the northwestern Pacific. It is found, antitropically, in separate popula-
tions in all oceans. Most populations have been named as species or subspecies at
some time in the past: japonicus Houttuyn, 1782, from Japan; colias Gmelin,
1789, from the eastern Atlantic; grex Mitchill, 1815, from the western Atlantic;
diego Ayres, 1857, from the northeastern Pacific; peruanus Jordan and Hubbs,
1925, from the southeastern Pacific; and marplatensis Lopez, 1935, from Argen-
tina. Recent molecular evidence (see Section II) combined with morphological
data convinced Collette (1999) to recognize the Atlantic S. colias as a distinct
species, separate from the Indo-Pacific S. japonicus.
Because both S. japonicus and S. australasicus possess swim bladders, the
generic name Pneumatophorus Jordan and Gilbert, 1883, meaning swim-bladder
bearer, has been used to distinguish them from S. scombrus, which lacks this or-
gan. However, more recent authors (Fraser-Brunner, 1950; Collette and Gibbs,
1963; Matsui, 1967; Collette, 1979) have considered Pneumatophorus a synonym
of Scomber. In addition to having lost its swim bladder, S. scombrus differs from
S. juponicus and S. australusicus in several other morphological characters: S.
scombrus has 13 + 18 vertebrae instead of 14 + 17, has the first haemal spine
anterior to the first interhaemal bone, has more heavily ossified bones (Matsui,
1967, Table 5>, and has a very different otolith morphology from the other two
Scomber taxa (Fitch and Craig, 1964). This suggests that the earlier division of
Scomber into two genera, one containing S. scombrus and the other containing
S. japonicus and S. australasicus, is a hypothesis that can be tested with molecu-
lar data.
1. SYSTEMATICSOFTHETUNASANDMACKERELS 7
Rastrelliger Jordan and Starks, 1908, was described as differing from Scomber
in having larger scales, more numerous and more elongate gill rakers, and a more
compressed body. However, description of a third species in the genus made these
differences less definite, and it became necessary to rely on anatomical characters
to distinguish the genera. Matsui (1967, Table 4) summarized the diagnostic
characters of Rastrelliger, which include a toothless vomer and palatines, last
branchiostegal ray flattened and forming a wide plate (Matsui, 1967, Figure 3)
rudimentary anal spine, 11 interneural bones under the first dorsal fin, first inter-
haemal bone anterior to the haemal spine of the 14th vertebra, and first haemal
spine flattened and hooklike. The number of vertebrae are 13 precaudal plus 18
caudal.
There are three species of Rastrdliger according to Matsui (1967)-R.
faughni Matsui, 1967, from Taiwan, the Philippine Islands, and Indonesia; R. bra-
chysoma Bleeker, 1851, in the same general area of the western Pacific as R.
faughni but extending east to Fiji; and R. kanagurtu Cuvier, 1817, which is wide-
spread throughout the Indo-West Pacific from Taiwan, the Philippines, Samoa,
and Australia, east throughout the Indian Ocean to Madagascar and the Red Sea.
At least one individual has gone through the Suez Canal into the eastern Mediter-
ranean Sea (Collette, 1970). Matsui (1967, Table 2) summarizedcharactersdistin-
guishing the three species: number of gill rakers, length of the intestine (about
equal to the length of the fish in R. fuughni, 1.3 -1.7 times longer in R. kanagurta,
and 3 -3.4 times longer in R. brachysoma), number of bristles on the longest gill
raker, and body depth.
2. TRIBE SCOMBEROMORINI BARKS, rglo

This is the most speciose tribe in the family, containing 21 of the 50 species.
Most of these are the 18 species of Scomberomorus, the Spanish mackerels and
seerfishes; the other 3 species belong to the monotypic genus Acunthocybium and
to Grammatorcynus. Scomberomorini have large compressed teeth which are ser-
rate in some species. As in higher scombrids, there is a well-developed median
keel on the caudal peduncle, but there is no bony support as is present in the
Sardini and Thunnini.
a. Grammutorcynus Gill, 1862. This Indo-West Pacific genus differs from

Scomberomorus in having two lateral lines, a pineal window, a single interpelvic
process, fewer vertebrae, a well-developed swim bladder, and larger scales. It has
the same number of vertebrae as do the Scombrini (3 l), usually 13 precaudal plus
18 caudal. Possession of an extra, ventral lateral line is unique in the family. John-
son (1986, Figure 1) placed Grummatorcynus in the middle of his cladogram,
sister to Sardini, Thunnini, Scomberomorini, and the billfishes. Here, the genus is
considered to be the plesiomorphic sister group of Scomberomorus + Acantho-
cybium. Long thought to be monotypic, the genus contains two species (Collette
8 BRUCE B. COLLETTE ET AL.
and Gillis, 1992). The double-lined mackerel G. bilineatus Rtippell, 1836, is wide-
spread in the tropical Indo-West Pacific, particularly near coral reefs from the
Marshalls and Carolines, Philippine Islands, Australia, and the East Indies, west
to the Red Sea. The shark mackerel, G. bicarinatus Quoy and Gaimard, 1825, has
a smaller eye, fewer gill-rakers, and several osteological differences. It is restricted
to the northern three-quarters of Australia and the Gulf of Papua.
b. Scomberomorus Lacepede, 1801. As many as seven subgenera of Scom-

beromorus were recognized by Munro (1943), exclusive of Lepidocybium, which
belongs to the Gempylidae, and Cybiosarda, which is a member of the Sardini.
Fraser-Brunner divided the genus into only two subgenera, Cybium with two spe-
cies (cavalla and commerson) and Scomberomorus with seven species. Mago Lec-
cia (1958) also noted the close relationships of S. cavalla and S. commerson.
Fraser-Brunner placed a number of valid species in synonymy, and new species
have been described since then. Scomberomorus differs from the other two genera
in the tribe, Acanthocybium and Grammatorcynus, by lacking a swim bladder.
Scomberomorus also lacks the extra lateral line present in Grummatorcynus and
the elongate snout characteristic of Acanthocybium.
There are 18 species in the genus (Collette and Russo, 1985b): 1 species in
the Gulf of Guinea and Mediterranean Sea (S. tritor Cuvier, 1832); 4 in the west-
ern Atlantic (cavullu Cuvier, 1829; regalis Bloch, 1793; maculatus Mitchill,
1815; and brusiliensis Collette, Russo, and Zavala-Camin, 1978); and 2 in the
eastern Pacific (concolor Lockington, 1879, and sierra Jordan and Starks, 1895).
The remaining species are Indo-West Pacific: guttatus Bloch and Schneider,
1801; koreanus Kishinouye, 1915; lineolatus Cuvier, 1832; plurilineatus Four-
manoir, 1966; commerson Lacepede, 1800; sinensis Lacepbde, 1800; semifuscia-
tus Macleay, 1883; queenslandicus Munro, 1943; niphonius Cuvier, 1832; munroi
Collette and Russo, 1980, from Australia and New Guinea; and multirudiatus
Munro, 1964. This last species has the most restricted range of any member of the
family; it is known only from off the mouth of the Fly River in Papua New Guinea.
Meristic characters of value at the specific level in Scomberomorus include
numbers of gill rakers, dorsal spines, dorsal and anal fin rays, vertebrae, and intes-
tinal folds (Collette and Russo, 1985b). Dips in the lateral line and the locations
of these dips distinguish S. cavalla, S. commerson, and S. sinensis. Fine branches
extend off the anterior part of the lateral line in S. guttutus and S. koreanus.
A number of morphometric characters are useful in separating species-head
length, body depth, pelvic fin length, heights of second dorsal and anal fins, width
of the median caudal peduncle keel, etc. Adult color pattern is also important in
this genus; there are barred species (cavalla, commerson, and semifasciatus), spe-
cies with variously interrupted horizontal lines (regalis, lineolatus, andplurilinea-
tus), species with spots of varying sizes and numbers (maculatus, sierra, tritou,
guttatus, koreanus, niphonius, queenslandicus and sinensis), and species with es-
1. SYSTEMATICSOFTHETUNASANDMACKERELS 9
sentially no markings at all (colacolor and multirudiatus). The number of gill rak-
ers ranges from 1-4 in S. multiradiatus to 21-27 in S. concolor. Vertebrae range
from as low as (19 to 20) + (20 to 22) = 39 to 42 in S. sinensis to as high as (20
to 21) + (35 to 36) = 55 to 56 in S. multirudiatus.
One well-defined monophyletic group of species within the genus is the re-
galis group (Collette and Russo, 1985b). This group is defined by the presence of
nasal denticles-teeth in the nose. Characters of the anterior arterial system, pel-
vic girdle, and skull define groups within the regalis group. The phylogeny con-
structed from morphological characters can be compared with the distributions of
the species. Collette (1999, Figure 10) shows a cladogram inferred from species
distributions which is identical to that based on morphology (Collette, 1999, Fig-
ure 9). Both trees show 5. reguZis and S. brasikensis being most closely related,
with S. sierra as the sister taxon to this pair, followed by S. concolor. Scombero-
morus tritor was the most plesiomorphic species.
Host-parasite relationships of parasitic copepods were utilized to provide an
independent assessment of relationships of Spanish mackerels of the S. regalis
species group (Collette and Russo, 1985a). Clustering of the hosts based on hy-
pothesized parasite relationships resulted in a slightly different tree, with the two
eastern Pacific species, concolor and sierra, showing closer relationships than in
the morphology-based tree. The differences between the tree based on mor-
phology and one derived from host-parasite relationships suggest that a discrep-
ancy exists, and this can be examined further using molecular data.
c. Acanthocybium Gill, 1862. This monotypic genus appears to be a special-

ized offshoot of Scomberomorus and does not merit placement in its own sub-
family or tribe as has been advocated by previous authors such as &arks (1910).
The wahoo, A. solundri Cuvier, 1831, is a large species (reaching over 1500 mm
SL) and has a well-developed swim bladder. It is a high seas epipelagic species
found around the world in tropical and subtropical waters. It is closest to the Cv-
bium group of Scomberomorus (S. cavulla and S. commerson) according to Con-
rad (1938), Mago Leccia (195X), and Collette and Russo (1985b). Johnson (1986)
presented an alternative hypothesis of scombroid relationships in which the wahoo
was placed between Spanish mackerels and billfishes. The wahoo has lost all its
gill rakers, the gill filament blades are interconnected by an extensive latticework
of cartilaginous bridges invested with tooth plates, the number of vertebrae has
increased to over 60, and its snout and jaws are elongate and beaklike. However,
in both hypotheses, numerous reversals and independent acquisitions must have
occurred no matter where billfishes are placed (Carpenter et al., 1995).
3. TRIBESARDINIJORDANANDEVERMANN,~ 896
The bonitos are a grade of seven species placed in four genera (Collette and
Chao, 1975; Collette, 1999). They differ from the more primitive mackerels and
Spanish mackerels in lacking a notch in the hypural plate and in having a bony
keel to support the median fleshy keel on the caudal peduncle. Prom the tunas,
they differ in having the bony keel only partially developed, in lacking any coun-
tercurrent heat exchange system, and in lacking a pair of dorsally projecting car-
tilaginous ridges on the upper surface of the tongue. Sardini lack the prominent
paired frontoparietal foramina characteristic of all Thunnini except Auk. Sar-
dini differ from Thunnini in lacking prominent prootic pits on the ventral surface
of the cranium and complete centralization of the slow-oxidative muscle. Sardini
lack any known synapomotphies, so from a cladistic point of view the group
should be combined with Thunnini. There are some practical advantages of
keeping bonitos separate from tunas so the tribes are maintained here. Collette
and Chao (1975, Table 14) have summarized characters distinguishing genera of
Sardini.
a. Orcynopsis Gill, 1862. The monotypic genera Orcynopsis and Cybiosarda

share several characters that distinguish them from Sarda and Gymnosarda: low
and poorly developed bony caudal peduncle keels versus well-developed keels
divided into anterior and posterior sections on each preural vertebra; the right lobe
of the liver being longest versus the right and left lobes much longer than the
middle lobe; and the spleen small and concealed under the liver in ventral view
versus large and prominent in ventral view. Orcynopsis, Cybiosarda, and Gym-
nosarda have two patches of tongue teeth, but the patches are attached to the
glossohyal bone in the former two genera and are on separate plates that fit over
the bone in Gymnosarda. Orcynopsis differs from Cybiosarda most obviously by
lacking the bold pattern of stripes and blotches of the latter. Orcynopsis has fewer
fin rays, ribs, and vertebrae than Cybiosarda. Orcynopsis is a short-bodied and
short-headed bonito. Orcynopsis unicolor Geoffrey St. Hilaire, 1817, is an eastern
Atlantic endemic whose range is centered in the Mediterranean Sea but extends
south to Dakar, Senegal, and north to Oslo, Norway (Collette and Chao, 1975,
Figure 69).
b. Cybiosarda Whitley, 1935. As noted above, the monotypic genera Cybio-

sarda and Orcynopsis share a suite of characters that differentiate them from
Sarda and Gymnosarda. Cybiosarda is the most conspicuously marked scombrid,
with a prominent pattern of black spots over a deep blue background above the
lateral line, dark stripes on the light venter reminiscent of the skipjack Katsu-
wonus, a high first dorsal fin that is jet black anteriorly and pure white posteriorly,
and yellow dorsal and anal fins. Cybiosarda has more fin rays, ribs, and vertebrae
than Orcynopsis. Cybiosarda &guns (Whitley, 1935) is virtually an Australian
endemic found along the northern three-quarters of the continent from Perth,
Western Australia, to Sydney, New South Wales (Collette and Chao, 1975, Figure
69) and also along the south coast of Papua New Guinea.
1. SYSTEMATICS OF THE TUNAS AND MACKERELS 11
c. Surda Cuvier, 1829. The four species of Surda all have several dorsal
stripes, ranging from horizontal to oblique in orientation. Sarda and Gymnosarda
share a number of characters that distinguish them from Orcynupsis and Cybio-
sarda: the bony caudal keels are well developed as in Thunnini but are divided
into anterior and posterior sections on each vertebra; the spleen is large and promi-
nent in ventral view versus small and concealed; and the right and left lobes of the
liver are longer than the middle lobe versus the right lobe being the longest. Sarda
resembles Allothunnus and differs from other genera of bonitos in having the in-
testine run straight from the stomach to the anus (instead of having two additional
loops) and having two intermuscular bones per side attached to the rear of the
skull (Gymnosardu has none, and the other three genera have one per side).
Collette and Chao (1975) recognized four species of Sardu: S. austrulis
Macleay, 1881, is restricted to the east coast of Australia plus Norfolk Island; S.
chiliensis inhabits the eastern Pacific, where it is divisible into two subspecies,
S. c. chiliensis Cuvier, 1832, from Peru and Chile, and S. c. lineolata Girard, 1859,
from Alaska to Baja California; S. orientalis Temminck and Schlegel, 1844, is
widespread in the Indo-Pacific from South Africa and the Red Sea, east to Japan,
China, the Philippine Islands, and the Hawaiian Islands, and across into the east-
ern Pacific from Baja California to Peru; and S. sarda Bloch, 1793, is found
throughout tropical and temperate waters of the Atlantic Ocean, including the
Gulf of Mexico and the Mediterranean and Black seas (Collette and Chao, 1975:
Figure 70).
A summary of the 26 most important characters used in distinguishing species
of Sardu has been presented by Collette and Chao (1975, Table 17). Meristic
characters include numbers of nasal lamellae, upper and lower jaw teeth, gill rak-
ers, ribs, vertebrae, dorsal fin spines, anal fin rays, dorsal and anal finlets, and
pectoral fin rays. There are a number of osteological differences in various bones.
Morphometric differences have also been summarized (Collette and Chao, 1975,
Table 18).
d. Gymnosarda Gill, 1862. The monotypic genus Gymnosarda differs from

other bonitos in having a well-developed swim bladder, in lacking intermuscular
bones on the rear of the skull, and in having more lamellae in the olfactory rosette
(48-56 vs. 21-39 in the other Sardini). Gymnosarda is the only bonito with 19
precaudal and 19 caudal vertebrae. It has a differently shaped head-larger eyes,
wider interorbital distance, shorter postorbital distance, and more elongate oper-
cular bones. As noted above, Gymnosarda and Sardu share several characters that
distinguish them from Orcynopsis and Cybiosarda. Gymnosarda differs from
Surdu in lacking scales on the body posterior to the corselet, having a pair of tooth
plates on the tongue, lacking the stripes characteristic of Surdu, and having a loop
in the intestine. Gymnosardu unicolor (Riippell 1836), the dogtooth tuna, is a
coral reef species of the tropical Indo-West Pacific (Collette and Chao, 1975, Fig-
12 BRUCE Et. COLLETTE ET AL.
ure 69). Its large eyes and teeth, numerous olfactory lamellae, and well-developed
swim bladder suggest that it may be more of a lurking predator on larger fishes
than are other bonitos.
4. TRIBE THUNNINI STARKS, 1910
Four genera of tunas were included in Thunnini by Collette (1979), but later
Allothumus was added as the most primitive member of the tribe. The four genera
are unique among bony fishes in having a countercurrent heat exchanger system
of retia mirabiha in the circulatory system. A similar system has evolved indepen-
dently in lamnid sharks (Carey et aZ., 1971). The rete mirabilia provide the vas-
cular mechanism for conserving metabolic heat in the muscle, viscera, and brain
of tunas and lamnid sharks. This permits the fish to maintain body tissue tempera-
tures warmer than the surrounding water. The three more primitive genera (Auk,
Euthynnus, and Katsuwonus) and the three members of the subgenus Neothunnus
(Thunnus albacares, Thunnus tonggol, and Thunnus atlanticus) have central as
well as lateral heat exchangers; the cold-water members of the subgenus Thunnus
(bluefins, bigeye, and albacore) have no central heat exchanger and have evolved
a well-developed lateral heat exchanger (Carey et al., 1971; Graham, 1973, 1975).
In addition, the cold-water Thunnus have visceral and cranial retia mirabilia.
Thunnini are the only scombrids with a pair of dorsally projecting ridges on the
upper surface of the tongue. The bony keels on the caudal peduncle vertebrae
are completely developed rather than only partially developed as in the Sardini.
Thunnini, except Allothunnus and Auk, have a prominent pair of frontoparietal
foramina on the dorsal surface of the skull. All Thunnini have well-developed
prootic pits on the ventral surface of the skull.
a. Allothunnus Serventy, 1948. The monotypic Allothunnus differs from all

other scombrids in its very high number of gill rakers. Allothunnus differs from
all other scombrids in having the prootic bones remarkably extended laterally as
wings that frame the posterior margin of the orbit. Allothunnus resembles other
Thunnini and differs from Sardini in having a prootic pit in the ventral surface of
the skull. The pineal window is large and oval in Allothunnus, and elongate and
slit-shaped in the Thunnini and Sardini. The liver has three subequal lobes as in
the bluefin species group of Thunnus. Recent studies on the morphology of Allo-
thunnus by Graham and Dickson (2000) confirm its position as the most primitive
member of the Thunnini because it has a highly modified central circulation (heat-
exchanging aorta postcardinal vein, and associated branch vessels) similar to the
central heat-exchanging retia of tunas, and enlarged haemal arches and anterior,
internal placement of red muscles as in tunas. Allothunnus fallui Serventy, 1948,
the slender tuna, is found around the world in the Southern Ocean south of 35”s
(Collette and Chao, 1975, Figure 69), with two highly unusual records from the
North Pacific, one from the Los Angeles-Long Beach harbor complex (Fitch and
Craig, 1964) and the second from the North Pacific subarctic gyre at 44” N, 15 1o W
(Schaefer and Childers, 1999).
b. Auxis Cuvier, 1829. After Allothunnus, Auk is the next most primitive
genus of the Thunnini. It lacks the prominent frontoparietal foramina found in the
three genera of higher tunas, Euthynnus, Katsuwonus, and Thunnus. Dorsal and
ventral branches of the cutaneous artery originate separately in Auxis (Godsil,
1954); a common cutaneous artery divides into dorsal and ventral branches lateral
to the aorta in the other three genera. The ventral branch is very poorly devel-
oped-less so than in the three more advanced genera. In Auxis the dorsal cuta-
neous artery lies ventral to the corresponding vein, versus dorsal in Euthynnus
(Godsil, 1954). The vertebral column differs from all other scombrids in having a
long pedicel or epihaemal process which forces the dorsal aorta to run much fin-
ther ventrally from the vertebral column (1.5 -2 times the centrum depth) than in
other tunas. Auxis shows no suturing of the first vertebra to the skull as is present
in higher Thunnini. Auks has a single huge interpelvic process which is about
equal to the pelvic fins in length. Auxis resemble Scomber in having a long dis-
tance between the dorsal fins. The liver is similar to that in Euthynnus in having a
very long right lobe running the length of the body cavity. Prominent branches of
the hepatic vein are present on the ventral surface of the liver lobes in both genera.
Auxis differs from Euthynnus in having a greatly reduced left liver lobe; the left
and middle lobes are of about equal length in Euthynnus. The swim bladder is
absent and the body is naked posterior to the corselet, as in Euthynnus and Kat-
SUWOI~US. There are a total of 39 vertebrae as in Thunnus and some species of
Euthynnus-20 precaudal plus 19 caudal. Gill rakers range from 37 to 47 in
number.
There are two species of frigate tunas (Collette and Aadland, 1996): the nar-
row-corseleted A. thazard (Lacepede, 1800) and the wide-corseleted A. rochei
(Risso, 18 10). In both species an extension of the corselet follows the lateral line
posteriorly. In A. thazard the extension is only 1-5 scales wide beneath the second
dorsal fin; in A. rochei it is 6 scales or more. This difference is correlated with a
difference in number of gill rakers, 37-43 (mean about 40) in A. thazard and 40 -
47 (mean about 45) in A. rochei. Both species are widely distributed in tropical
and subtropical waters of the Indo-Pacific. The two species were clearly distin-
guished in the Pacific by Kishinouye (1923) Wade (1949), and Matsumoto
(1960), under a variety of names. Occurrence of both species in the Atlantic was
not confirmed until recently (Richards and Randall, 1967; Collette and Aadland,
1996). Frigate tunas are the smallest of the tunas, A. rochei reaching 500 mm FL
and A. thazard at least 580 mm FL. Eastern Pacific populations of both species
differ morphologically from populations in the rest of the world, leading Collette
and Aadland (1996) to describe them as subspecies. The eastern Pacific A. thaxzrd
brachydorax Collette and Aadland, 1996, has more gill rakers than the widespread
14 BRUCE B. COLLETTB ET AL.
A. t. thazard, usually 43-48 versus 38-42, and also differs in several morpho-
metric characters. The eastern Pacific A. rochei eudorax Collette and Aadland,
1996, has an even wider corselet than that of A. r. rochei-usually more than
20 scales wide compared with 6 - 19 scales.
c. Euthynnus Ltitken in Jordan and Gilbert, 1882. Euthynnus is closely related

to both the more primitive Auxis and the more advanced Katsuwonus. Some re-
searchers (Fraser-Brnnner, 1950; Collette and Gibbs, 1963) placed Katsuwonus in
synonymy with Euthynnus, but this obscures the relationships of Euthynnus sensu
strict0 with Auxis and of Katsuwonus with Thunnus. Euthynnus differs from Auxis
in having a common trunk for the dorsal and ventral branches of the cutaneous
artery. It is less advanced than Katsuwonus because the ventral branch of the cu-
taneous artery is short and dendritic (Godsil, 1954), and much less developed than
the dorsal branch. In Euthynnus the dorsal cutaneous artery lies dorsal to the cor-
responding vein, and not ventral as in Auxis. The trelliswork on the vertebral col-
umn moves the aorta ventrally a distance greater than the depth of the centmm-
less than in Auks and more than in Katsuwonus. Euthynnus is similar to Auxis and
Katsuwonus in lacking a swim bladder and in having the body naked posterior to
the corselet. Euthynnus resembles Auxis in having the right lobe of the liver ex-
tending the length of the body cavity and in having prominent hepatic veins on
the ventral surface of the liver. It differs from Auxis in having a much longer left
lobe that is about equal in length to the middle lobe. Katsuwonus has a much
shorter and narrower right lobe and lacks hepatic veins on the ventral surface of
the liver. Euthynnus resembles Katsuwonus in having the upper half of the first
vertebra sutured to the skull-more than in Auxis but less than in Thunnus. The
number of vertebrae is 37-39, fewer than in Katsuwonus (41).
There are three allopatric species of Euthynnus: E. alletteratus Rafinesque,
1810, in the Atlantic; E. a&is Cantor, 1849, throughout the Indo-West Pacific;
and E. lineatus Kishinouye, 1920, in the eastern Pacific. There is a valid record
of E. afiis from the eastern Pacific (Godsil, 1954, 139) and two of E. lineatus
from the Hawaiian Islands (Matsumoto and Kang, 1967; Matsumoto, 1976). God-
sil(1954, Table 17) summarized the characters that differentiate the species (with
E. afinis as E. yaito): vomerine teeth (absent only in E. alletteratus); gill rakers
(29-33 in E. afinis, 33-39 in E. lineatus, and 37-40 in E. alletteratus); vertebrae
(37 in E. lineatus and 39 in the other two species); vertebral protuberances (ab-
sent in E. a&is, incipient on 33rd and 34th vertebrae in E. alletteratus, and four
large lobes on the 3 1st and 32nd vertebrae in E. line&us); and location of caudal
keels (on 31st and 32nd vertebrae in E. lineatus, and 33rd and 34th in the other
two species). Species of Euthynnus characteristically, but not invariably, have a
variable number of black blotches on the sides between the pectoral and pelvic
fins. Gill rakers range from 29 to 40 in number, many fewer than in Katsuwonus
(53-63).
d. Kutsuwonus Kishinouye, 1923. This monotypic genus is most closely re-

lated to Euthynnus and Thunnus. It is more advanced than Euthynnus in having
the dorsal and ventral branches of the cutaneous artery about equally developed
instead of having the ventral branch short and dendritic (Godsil, 1954). Trellis-
work on the vertebral column moves the aorta ventrally a distance slightly less
than the depth of a centrum-less than in Auxis and Euthynnus, and more than in
Thunnus. The liver resembles that of the yellowfin group of Thunnus more than
that of Euthynnus and Auxis, because the right lobe does not extend the length of
the body cavity and hepatic veins are absent from the ventral surface of the liver.
Kutsuwonus resembles Auxis and Euthynnus and differs from Thunnus in having
the body naked posterior to the corselet. Kutsuwonus has more vertebrae than
Thunnus (41 compared to 39). Kutsuwonus resembles Euthynnus in having only
the upper half of the first vertebra sutured to the skull compared to completely
sutured in Thunnus. As in Auxis and Euthynnus, no swim bladder is present and
the intestine is straight, without folds. Kutsuwonus pelamis Linnaeus, 1758, the
skipjack, is a moderate-sized species of tuna reaching about a meter in length and
a weight of 18 kg (rarely as high as 23 kg). It has a striking pattern of dark longi-
tudinal stripes on the ventral half of the body. It has many gill rakers, with 53-63
on the first arch. It is cosmopolitan in tropical and subtropical seas.
e. Thunnus South, 1845. This, the most advanced genus of Scombridae, con-
tains eight species. Thunnus is more specialized than other genera of Thunnini in
having more pectoral fin rays (30-36 vs. 23-27) and in having the first vertebra
completely sutured to the skull. Thunnus has fewer vertebrae than Kutsuwonus
(39 vs. 41). Posterior to the corselet, the body is covered with small scales, com-
pared to being naked in the other genera of Thunnini. A swim bladder is present
in all the species except r tonggol. The intestine has an additional loop in it that
is not present in the other four genera. While vertebral trelliswork is present in
Euthynnus and Kutsuwonus, it is reduced (yellowfin species group) or absent
(bluefin group) in Thunnus.
A number of workers (e.g., Kishinouye, 1923; Godsil and Byers, 1944)
divided Thunnus into several genera, reaching an extreme of six genera for the
seven species then recognized. Gibbs and Collette (1967) placed the nominal gen-
era Purathunnus (for bigeye), Neothunnus and Semathunnus (for yellowfin),
Germo (for albacore), and Kishinoellu (for longtail) in the synonymy of Thunnus
(based on bluefin). They argued strongly against subdividing Thunnus into genera
because reliance on different characters led to very different groups of species.
They did show that there were two groups of species with the bigeye tuna, I:
obesus, intermediate between the groups. Le Gall et al. (1976) performed a mul-
tivariate analysis on the data presented by Gibbs and Collette and confirmed their
findings that there are two groups of species, with 7: obesus intermediate. Le Gall
et al. (1976) concluded that it was useful to recognize three subgenera: Thunnus
for the bluefin group, Neothunnus for the yellowfin group, and Parathunnus for i?
obesus.
Collette (1979, 1999) divided the genus into two subgenera, Thunnus for the
cold-water clade-bluefins, southern bluefin, and albacore-and Neothunnus for
the tropical tunas-yellowfin, blackfin, and longtail. This classification was based
largely on morphological differences in adaptations for endothermy such as liver
morphology, vascularization, position of the cutaneous artery, and size of ventro-
lateral vertebral foramina. Species of Neothunnus possess both central and lateral
heat exchangers, although the lateral retia mirabilia are relatively small. Members
of Thunnus have their lateral retia highly developed, but the central heat ex-
changer has been lost or reduced, and this group also has additional retia which
function to elevate the temperature of their viscera, eyes, and brains. The major
differences between the two subgenera are associated with this loss of the central
heat exchanger in the bluefin group (Carey et al., 1971; Graham, 1975). With an
understanding of the adaptive significance of the differences in heat exchangers
between the two subgenera, TT:obesus seems best placed in the subgenus Thunnus.
$ Subgenus Neothunnus Kishinouye, 1923. This subgenus contains the three

tropical species of Thunnus which have central heat exchangers, as do the three
less advanced genera of Thunnini. Gibbs and Collette (1967,99) found that these
three species were similar to each other in 15-16 of 18 characters. No striations
are present on the ventral surface of the liver and no vascular retia mirabilia are
present on the dorsal surface. The postcardinal vein is present as in more primitive
Thunnini. Several structural modifications in the vertebral column permit the pas-
sage of more or larger blood vessels through the haemal arch, as Graham (1975)
has pointed out: the prezygapophyses arise more ventrad on the haemal arch, the
postzygapophyses are longer, and the interior foramina are larger (Gibbs and Col-
lette, 1967, Figures 10-13).
The three species in the subgenus Neothunnus are the blackfin tuna, Thunnus
adanticus (Lesson, 1831), of the western Atlantic (Martha’s Vineyard, MA, to Rio
de Janeiro); the longtail tuna, I: tonggol (Bleeker, 185 l), of the Indo-West Pacific
(Japan to Australia, and west through the Indo-Australian Archipelago to Somalia
and the Red Sea); and the yellowfin tuna, 7: albacares (Bonnaterre, 1788), a pan-
tropical species (Stoles and Graves, 1998). Thunnus atlanticus differs from other
species of Thunnus in having 19 + 20 vertebrae instead of 18 + 21. Both rI:
atlanticus and T. tonggol have few gill rakers (19-25 and 19-28, respectively).
Thunnus tonggo differs from other Thunnus in lacking a swim bladder. Other
differences are treated in detail by Gibbs and Collette (1967).
g. Subgenus Thunnus South, 1845. This subgenus contains the five larger spe-
cies of tunas which have been able to invade cooler waters due to their possession
of effective lateral heat exchangers. Gibbs and Collette (1967, 99) showed that
three species of this group resembled each other in 14 -16 of 18 characters. Stria-
tions caused by blood vessels are present on the ventral surface of the liver and
vascular cones are associated with the dorsal surface of the liver, indicating pres-
ence of a visceral heat exchanger. The three lobes of the liver are roughly equal in
length compared to the subgenus Neothunnus, where the right lobe is significantly
longer than the other lobes. The postcardinal vein has been lost in some members
but not all (present but reduced in size in 7: obesus). The vertebral column shows
no special modifications that would facilitate passage of more or larger blood
vessels through the haemal arch; the prezygapophyses arise on the centra, the
postzygapophyses are short, and the interior foramina are small.
Based on morphology, four species clearly belong to this subgenus: the Atlan-
tic and Pacific bluefin tunas ‘I: thynnu~ (Linnaeus, 1758), and T. orientalis (Tem-
minck and Schlegel, 1844); the southern bluefin tuna r maccoyii (Castelnau,
1872); and the albacore 7: aldunga (Bonnaterre, 1788). The fifth species, the
bigeye tuna ZYobesus (Lowe, 1839), is intermediate between the subgenera, shar-
ing 12 characters with T. maccoyii and 10 with T. albacures (Gibbs and Collette,
1967,99). The bigeye tuna matches with the subgenus Thunnus in the important
liver and vertebral characters; however, it is similar to Neothunnus with respect to
the position where the cutaneous artery originates from the aorta and where it
divides into dorsal and ventral branches. Because it has lost the central heat ex-
changer, it is placed in the subgenus Thunnus, although it is morphologically the
most different of the five species in the subgenus.
Characters that distinguish species of the subgenus Thunnus and the distribu-
tions of the species are treated in detail by Gibbs and Collette (1967). All five
species are widespread. Bluefin tunas extend into temperate waters of the North
Atlantic (7: thynnus) and North Pacific (7: orient&is). The southern bluefin, I:
maccoyii, has a distribution pattern similar to that of Gusterochismu and Allothun-
nus in the Southern Ocean. Thunnus alulungu is found from 42”N to 32”s in the
Atlantic, 10”N to 30% in the Indian Ocean, and 50”N to 45% in the Pacific; how-
ever, most of the fisheries for it are concentrated in temperate waters. Thunnus
obesus has much the same latitudinal distribution as the yellowfin T ulbacares.
but it usually is found in deeper and cooler waters than the yellowfin.
Of the subgenus Thunnus, 7: ululungu has much longer pectoral fins than do
the other species; 7: thynnus, 7: orientalis, and 7: muccoyii have very short pector-
als. Thunnus thynnus, 7: orientalis, and 7: muccoyii have more gill rakers (3 l-43)
than do 7: alalunga and T. obesus (23-3 1). Thunnus ululunga has the spleen on
the right side of the viscera; the other species of the subgenus (and genus) have
the spleen on the left. Hence, ?: ulalungu is somewhat different from the other
species in the subgenus. This idea, along with others dealing with the number of
unique lineages of the genus Thunnus, is addressed in Section II.
18 BRUCE B. COLLETTE El-AL.
II. MOLECULAR SY STEMATICS
Scombroids are among the best-known fishes anatomically (Carpenter et al.,

1995) and this group should present the systematist with the opportunity to pro-
duce well-corroborated phylogenies using the varied types of phylogenetic tech-
niques currently available. However, despite extensive morphological efforts to
construct phylogenies of the scombroids, this has not been the case. Cladistic phy-
logenies have been unstable, have generated conflicting hypotheses of scombroid
relationships among various workers in the field, and have yielded multiple most-
parsimonious trees (Carpenter et al., 1995). Systematic relationships are often not
clearly resolved and the choice of accepted trees often rests on the selection of
outgroup species and the choice of phenotypic characters used to group taxa. As
molecular genetic techniques have become more common in systematics, the op-
portunity has arisen to test some of the hypotheses proposed in the scombroid
literature using characters known to be heritable. It was hoped these techniques
would resolve key issues in scombroid systematics. Unfortunately, these methods
have often.fallen short of expectations.
The use of molecular data in fishery biology and systematics has recently led
to notable progress. For example, mitochondrial DNA has been most useful for
identifying all eight species of the genus 17tunnus (Bartlett and Davidson, 1991;
Finnerty and Block, 1995; Chow and Kishino, 1995; Alvarado-Bremer et al.,
1996). Genetic recognition of species in this genus has been extremely valuable
to the study of early life stages because larval forms are challenging to identify
morphologically (Collette et al., 1984). Physiological traits, such as endothermy
in scombroid fishes, have been mapped onto molecular phylogenies to examine
the patterns of evolution along specific lineages (Block et al., 1993; Finnerty and
Block, 1995). Estimates of genetic divergence among populations can be used to
visualize patterns of gene flow and corridors of migration in highly migratory
species, like the swordfish (Reeb et al., 2000), which can be useful for fishery
management. While results of molecular studies have verified, rejected, or failed
to resolve phylogenies, more often than not the data have provided both morpho-
logical and molecular systematists alike with a new perspective and alternative
hypotheses to test, thus propelling the field forward.
Molecular fishery biology is still a young field and new ideas await discovery.
In the meantime, scombroid genetics and molecular systematics are made difficult
by the propensity of this group to undergo rapid bursts of speciation over time
(Finnerty and Block, 1995) or for hybridization to confuse the phylogenetic his-
tory (e.g., Chow and Kishino, 1995; Banford et al., 1999). Such phenomena are
not unusual in evolution and scombroids are no exception. Many groups, includ-
ing mammals, have experienced rapid bursts of speciation (e.g., bears; Waits et al.,
1999) and hybridization (e.g., European house mice: Sage et al., 1993), which
1. SYSTFiMATICS OF THE TUNAS AND MACKERELS 19
were first revealed by molecular data and eventually understood. In this section
we demonstrate six hypotheses established by morphological data and tested using
molecular techniques. Molecular systematics of scombroids has been challenging,
especially in resolving relationships among older lineages. We believe that the
biggest challenge faced by systematists in resolving the deeper scombrid lineages
with molecular data is to overcome the problems associated with the use of short
DNA sequences for phylogenetic analysis and the frequent occurrence of rever-
sion mutation (homoplasy).
A. Are Billfishes Scombroid Fishes?
There has been a debate in the morphological literature as to the exact rela-
tionships among billfishes, tunas, and other scombroids (Collette et al., 1984;
Johnson, 1986; Carpenter et al., 1995). Parsimony analysis of both nucleotide and
amino acid sequences generated from 590 base pairs (bp) of the cytochrome b
gene and a 628-bp segment of the lactate dehydrogenase b locus places the wahoo,
Acanthocybium solundri, within a monophyletic Scombridae, Gempylidae, Tri-
chiuridae clade, while billfishes are consistently placed as a sister group to this
clade (Block et al., 1993; Finnerty and Block, 1994, 1995). Parsimony analysis of
the mitochondrial ATPase 6 gene (using both nucleotide and amino acid se-
quences) confirms monophyly of the billfishes (Alvarado Bremer, 1994). Thus,
molecular data provide a clear phylogenetic signal supporting monophyly of bill-
fishes and is in support of the morphological placement of wahoo in Scombero-
morini (Collette and Russo, 1985b). Billfishes are genetically distinct from other
scombroids and possibly belong in a separate suborder (Finnerty and Block,
1995). The apparent similarity in billfish morphology to that of Scombridae
noted earlier is likely equivocal largely because many of the cladistic characters
that unite billfish with the Scombridae appear to be convergent or reversals (Car-
penter et al., 1995; Finnerty and Block, 1995) causing homoplasy in the morpho-
logical tree.
B. Is Gasterochismatinae a Sister Group to the Scombrinae?
The currently accepted phylogeny of Collette and Russo (1985a) shown in

Figure 1 places the subfamily Gasterochismatinae at the base of the Scombridae.
As discussed above, Block et al. (1993) and Finnerty and Block (1995) used DNA
sequences of cytochrome b to construct a phylogeny of billfishes, mackerels, and
tunas in which Gasterochisma melampus was included. Their tree provided the
first molecular evidence that Gusterochisma may not form a sister relationship to
the Scombrinae. Figure 2 shows the phylogenetic relationships among scombroid
fishes derived from a 5 15-bp sequence of cytochrome b (from Block et al., 1993)
Tatrapturuspffuagari
T&a@urus angustirostrts
Tatmpturus babna
51 Thunnus atlantbus
Thunnus albacaras
Katsuwonus pelamis
Auxisthamd
,I Euthynnus alletteratus
1~ExlJ~~~
ri
l-l
Albthunnus
Lapkbcybium
failai
Gastmxhrna mafampus
flavobrunnaum
93 ’ scomberjaponicus
61 Scornbar scombtus
.Trichiurus lapturus
Ganqqiussarpans
66 Boombwomotus rnaculata
Scombemmorus cavalla _
Coryphasna aquisalis
0.05 changes
Fig. 2. Cytochrome b phylogeny for selected tunas, bonitos, mackerels, and billfish from data
from Block et al. (1993), Finnetty and Block (1995) Chow (unpublished), and Reeb and Block (un-
published). Neighbor-joining tree drawn with 515 bp using maximum likelihood distance. Values on
the nodes of branches are the percentage of bootstrap values out of 1000 replicates. Only values greater
than 50% are shown. Transition: transversion ratio is 10. Outgroup is Coryphaena equiselis.
along with two sequences from Chow for Thunnus tonggol and Thunnus atlanti-
cus (unpublished; GenBank accession numbers T. atlanticus AF239963 and T.
tonggol AF239964). We have recently sequenced 5 15 bp of cytochrome b from
Allothunnus fallai for inclusion in this analysis.
The tree in Figure 2 is a neighbor-joining tree using maximum likelihood dis-
1. SYSTEMATICS OF TKE TUNAS AND MACKERELS 21
tance and rooted with Coryphuena equiselis. The same placement of Gastero-
chisma is obtained when any one of the billfish species is used as an outgroup
(data not shown). The position of Gasterochisma could only be supported as a
polytomy after bootstrap analysis that includes Scombridae, Trichiuridae, and
Gempylidae, but excludes billfishes. This lack of resolution of the relationships is
significant as it clearly highlights a major dilemma in scombroid molecular sys-
tematics. The cytochrome b gene is highly saturated and homoplasy obscures the
relationships at the nodes of the tree where the Scombridae underwent diversifi-
cation into its major taxonomic lineages. As noted below, transitions in the silent
nucleotide sites of the cytochrome b gene are saturated in comparisons of older
scombroid taxa. Thus, resolution of the deeper nodes where the Scombridae un-
derwent diversification is unclear. The exception to this is the divergence between
billfish and the rest of the scombroids. In this case, there are a number of amino
acids that change in addition to silent mutations, providing additional characters
to construct the tree (Finnerty and Block, 1995). One way to overcome the satu-
ration problem of the cytochrome b gene in the analysis of relationships among
tunas, bonitos, and mackerels is to sequence a more slowly evolving gene such as
the 16s ribosomal gene (rDNA) in mitochondria.
In Figure 3 the phylogenetic tree is constructed from a partial sequence (475
bp) of 16s ribosomal DNA using maximum likelihood distance and the neighbor-
joining algorithm. Thunnus and Tetrapturus sequences were obtained from Reeb
(1995), while the remainder were sequenced for this analysis (Reeb and Block,
unpublished). Striped marlin was used as the outgroup. This phylogeny again
places Gasterochisma within the Scombrinae, only this time it clusters with the
tuna-bonito clade with a bootstrap value of 71%. From both the 16s and cyto-
chrome b trees it is clear that Gasterochisrna does not form a sister relationship
outside the Scombrinae, but rather falls within the family. However, Figure 1
places Gasterochismatinae as sister taxon to Scombrinae (Collette and Russo,
1985a), thus rooting the phylogeny. The position of Gasterochisma as a sister
taxon to the Scombrinae has been somewhat controversial as some morphological
studies have used alternative characters and interpretations and placed it within
the Scombridae (e.g., Carpenter et al., 1995).
C. Can Molecular Phylogenies Resolve the Thunnini

and Sardini Tribes?
In Figure 1, Allothunnus has been placed as the most primitive member of the
tribe Thunnini, while Katsuwonus is considered the sister group to the genus
Thunnus (Collette and Russo, 1985a; Collette, 1999). Allozymes (Elliott and
Ward, 1995) and cytochrome b gene studies (Block et al., 1993; Finnerty and
Block, 1995) indicate that there is strong molecular support for monophyly of
Thunnus, but less for the relationships of Euthynnus, Katsuwonus, and Auks to
one another and to Thunnus. In the phylogenies shown in Figures 2 and 3, Allo-
.Thunnusobesus
100
Thunnus albacares
Thunnus alalunga
Ailothunnus fallai
Sarda chiliensis
Euthynnus alletteratus
~ Gymnosarda unicolor
Gasterochisma melampus
Scomberomorus maculata
Tetrapturus audax
- 0.01 changes
Fig. 3. The 16s phylogeny of selected tunas, bonitos, and mackerels from Reeb (1995) and Reeb
and Block (unpublished). Neighbor-joining tree drawn from 475 bp using maximum likelihood dis-
tance. Transition: transversion ratio is 2. Values on the nodes of branches are the percentage of boot-
strap values out of 1000 replicates. Only values greater than 50% are shown. Outgroup is Terrapturus
audax.
thunnus has been added, and neither the cytochrome b nor the 16s rDNA trees are
able to support the relationships proposed by morphology as bootstrap values fall
well below 50%. Furthermore, there is little support for the separation of Thunnini
from Sardini as even the 16s phylogeny shows a polytomy among the members
of the two tribes. It should be noted that while several morphological characters
can distinguish Thunnini as a good monophyletic group, the Sardini do not pos-
sesssuch characters. Thus, the morphological data are in agreement with the mo-
lecular data suggesting that there is minimal support for the recognition of two
phylogenetically distinct tribes.
D. Problems Caused by Partial Sequences and Homoplasy
Partial sequences of the cytochrome b gene of the maternally inherited mito-

chondrial DNA (mtDNA) are used routinely in systematic studies to resolve rela-
tionships at the species level. However, analysis of short DNA sequences
(<750 bp) has been shown to cause errors in estimates of evolutionary relatedness
among taxa due to a large variance in substitution rate (Martin et al., 1990).
Hence, longer sequences are preferable, especially when the sequence is of a pro-
tein-coding gene where not all sites are free to vary. Another complication is the
use of a molecular marker that evolves too quickly. This can lead to the loss of
phylogenetic information through back mutation or reversals (Irwin et al., 1991;
Meyer, 1994).
Evidence for homoplasy is apparent in the cytochrome b data of scombroids
both in unresolved trees and in saturation curves. Figure 4 is a plot of transi-
tions (purine-purine or pyrimidine-pyrimidine substitutions) against transver-
sions (purine-pyrimidine substitutions) for the cytochrome b and 16s sequences
in Figures 2 and 3. In Figure 4a, transitions appear to be saturated relative to
transversions in cytochrome 6. It is not unusual for saturation to be reached
quickly with transitions as these substitutions occur more frequently than trans-
versions (Irwin et al., 1991). However, in this case, the ratio of transitions to trans-
versions is roughly equal, especially for comparisons between the deeper nodes in
the scombrids such as Euthynnus, Katsuwonus, Auks, and Allothumus. In this
situation, increased homoplasy in transitions can mask the phylogenetic signal of
transversions, thus distorting the relationships among taxa in the deeper nodes of
the tree. Finnerty and Block (1995, Figure 4) made an attempt to recover the true
tree by weighting transitions and transversions based on their frequency of occur-
rence. However, the deeper nodes of the tree remained unresolved. Finnerty and
Block (1995) also constructed a phylogeny using only amino acid sequences in an
attempt to examine the deeper nodes. Because most of the mutations among scom-
brid taxa occur at the noncoding or silent third positions of codons, very few
amino acid changes are evident and again, the deeper nodes of the tree remained
unresolved.
Figure 4b is a saturation plot for the more slowly evolving 16s ribosomal gene
of mtDNA using taxa comprising the phylogeny in Figure 3 constructed from a
partial sequence (475 bp) of 16s ribosomal DNA (rDNA). This plot shows no
evidence of saturation. However, the relationships among many of the scombroid
taxa in Figure 3 remain poorly resolved. Although both the cytochrome b and 16s
data are limited in information, they do provide interesting insight into the evolu-
tion of the Scombridae that will emerge repeatedly as future research examines
the systematic hierarchy of these fish.
A
Transitions vs Transversions in the Cytochrome b Gene
90
80
I
.!! ‘0
‘55 60
G 50
b
L 40
2
E 30
z” 20
10
0
0 10 20 30 40 50 60 70 80
Number of Transversions
Transitions vs Transversions in the 16s Gene
“us
0 5 10 15 20 25 30 35 40
Number of Transversions
Fig. 4. Plot of the number of transitions versus transversions for (a) cytochrome b and (b) 16s
for the Scombridae taxa in Figures 2 and 3, respectively.
The lack of resolution in the molecular trees based on molecules might stem
from the possibility that the Scombridae have undergone recurrent bouts of rapid
speciation. It is clear that the moderately evolving cytochrome b gene evolves too
quickly to retain its phylogenetic information before homoplasy becomes a prob-
lem among the deeper nodes. However, the slowly evolving 16s sequences are
unable to mutate fast enough to distinguish each lineage as it arose; hence all
lineages appear to coalesce to the same ancestral node, not to a series of bifurcat-
ing sister taxa as the morphological hypotheses would predict. One exception is
the monophyletic Thunnus lineage. Because this genus is recently derived, it can
be distinguished from the other Scombridae with the faster evolving cytochrome
b sequence (discussed below). The results in Figures 2 and 3 strongly suggest that
the major lineages of Scombridae evolved during periods of rapid speciation,
making it difficult for characters that evolve slowly to accumulate enough syna-
pomorphies. Meanwhile, faster evolving characters appear to undergo reversions
over time. Thus the molecular data explain why reconstructing the systematic re-
lationships within this family using either molecules or morphology remains a
challenge for systematists. One way to better support the hypothesis that rapid
speciation has occurred is to analyze much longer sequences from many different
genes. This approach has been used to show that bears have undergone bouts of
rapid speciation events (Waits et al., 1999).
E. Are Thunnus Monophyletic‘?
Molecular data sets have shown robust support for the monophyly of the genus
Thunnus (Elliott and Ward, 1995; Finnerty and Block, 1995; Chow and Kishino,
1995; Alvarado Bremer et al., 1996), which is consistent with morphological hy-
potheses. As noted earlier in this chapter, Collette (1979) proposed that Thunnus
should be divided into two subgenera comprising the tropical Neothunnus (7: al-
bacares, 7: tonggol, and 7: atlanticus) and the more cold-tolerant Thunnus (27
thynnus, 7: maccoyii, 7: alalunga, and i? obesus). In a series of studies involving
both mitochondrial and nuclear genes (Sharp and Pirages, 1979; Chow and Inoue,
1993; Finnerty and Block, 1995; Elliott and Ward, 1995; Ward, 1995), the results
have not been concordant with the morphology. For instance, in four molecular
studies the albacore, 7: alalunga, was found to be the most divergent member of
the genus. This leaves Neothunnus and the remaining Thunnus taxa as a separate
group, thereby rejecting the morphological hypothesis that the subgenus Thunnus
is monophyletic. The issue of whether Neothunnus is monophyletic was not com-
pletely addressed in these early studies as neither the longtail (‘I: tonggol) nor the
blackfin (7: atlanticus) were available for analysis.
The study of Chow and Kishino (1995, Figure 4) was the first to include all
eight Thunnus species in a molecular phylogeny. Analysis of a short (292 bp).
highly conserved fragment of cytochrome b and a 400-bp fragment of the mito-
chondrial ATPase gene produced a phylogenetic clustering of the species of the

subgenus Neothunnus. However, the node of the Neothunnus clade was not sup-
ported by bootstrap analysis (values < 50%) in Chow and Kishino’s study. Alva-
rado Bremer et al. (1996, Figure 4) sequenced 450 bp of the rapidly evolving,
noncoding d-loop region of the mitochondrial DNA, and a maximum-parsimony
analysis was able to support Neothunnus as a monophyletic group with a bootstrap
value of 79%. Importantly, in this analysis, the subgenus Thunnus was not shown
to be monophyletic as Neothunnus fell within the Thunnus subgenus. Interest-
ingly, both studies showed that the bigeye (T. obesus) clustered weakly with the
tropical Neothunnus and not its hypothesized Thunnus relatives, thereby compli-
cating the generic subdivision based on warm- and cold-water preferences. As
noted earlier, the bigeye tuna appears to be intermediate between Neothunnus and
Thunnus based on morphological characters (Gibbs and Collette, 1967, 99; Le
Gall et al., 1976).
F. Has Mitochondrial Introgression Occurred

between Bluefin and Albacore Tuna‘?
Two mitochondrial studies of the Thunnus genus discussed above show a sur-
prisingly close relationship between albacore (7: alulungu) and Pacific bluefin (r
orientalis), while the Atlantic bluefin (T. thynnus) and southern bluefin (Z muc-
coyii) group together as their vernacular names imply. Chow and Kishino (1995)
explain the sequence similarity between albacore and Pacific bluefin by interspe-
cific transfer of mtDNA, with’ albacore mtDNA introduced by hybridization re-
placing most of the original mitochondrial lineages in the Pacific bluefin. If this
explanation is correct, it is a case of horizontal rather than vertical evolution and
should not be a factor in deciding taxonomic status of Pacific bluefin.
Gibbs and Collette (1967) felt that the morphological differences between
southern bluefin on the one hand (first ventrally directed parapophysis on the 9th
vertebrae, yellow caudal keels) and Atlantic and Pacific bluefins on the other (first
ventrally directed parapophysis on the 10th vertebrae, dark caudal keels) were
strong enough to support species status of the southern bluefin. However, they
argued that the slight differences between Atlantic and Pacific bluefins (shape of
the dorsal wall of the body cavity in large specimens and numbers of gill rakers)
justified recognition of these two only as subspecies, I: thynnus thynnus and 7:
thynnus orientalis, respectively. Ward et al. (1994), Chow and Kishino (1993,
and Alvarado Bremer et al. (1996) have provided molecular data supporting the
division of bluefin into three taxonomic groups. In light of this newer molecular
data along with the morphological distinctions, although slight, between Atlantic
and Pacific bluefins, Collette (1999) now advocates separation of these bluefins
into Atlantic, 1: thynnus, and Pacific, 7: orientalis, species.
G. Can Molecular Data Resolve the Relationships

among Spanish Mackerels?
Collette (1999) noted a discrepancy in the phylogenies of Spanish mackerels

when morphology or species distributions were used to construct the tree versus
when host-parasite relationships were used. In an effort to determine which tree
better approximates phylogeny, Banford et al. (1999) reexamined the relation-
ships of the regalis group using both nuclear and mitochondrial DNA with the
Indo-Pacific Scomberomorus guttatus as the outgroup. The regalis group is mono-
phyletic and the Gulf of Guinea species, Scomberomorus tritor, is confirmed as
the most plesiomorphic sister species to the five American species. The Atlantic
Spanish mackerel, Scomberomorus muculatus, could not be distinguished from
Scomberomorus regalis on the basis of their mtDNA sequences due to mitochon-
drial introgression. The nuclear-encoded aldolase sequence strongly supported the
distinctiveness of S. maculatus and S. regalis, and the basal position of S. macu-
latus within the New World species. The two eastern Pacific species, concolor and
sierra, appear closely related to each other, similar more to the hypothesis gener-
ated from the parasite data than to that from the morphological data.
H. Is Scomber scombrus Generically Different from

Scomber japonicus and Scomher australasicus?
Stoles et al. (1998, Figure 5) used 418 bp of cytochrome b sequence and a

parsimony algorithm to generate a consensus tree rooted with Rastrelliger kuna-
gurta to show that S. ,japonicus and S. australasicus cluster together and away
from S. scombrus. Agreement of morphological and molecular data led Collette
(1999) to support division of Scomber into two genera or subgenera.
The genetic data also reveal an interesting problem. The tree in Stoles et al.
(1998, Figure 5) shows that S. japonicus and S. australasicus do not form separate
monophyletic clades. This conflicts with what was observed in an earlier study of
nuclear allozymes that showed fixed differences between a limited sample of the
two species (Kijima et al., 1986). Instead, the mtDNA tree shows three major
lineages, S. japonicus, S. australasicus, and one containing individuals of both
species. This suggests the possibility of hybridization after the speciation of S.
japonicus and S. australasicus (Stoles et al., 1998). Biparentally inherited nuclear
genes in the hybrid might retain a bit of the phylogenetic history of both paternal
and maternal ancestries while the maternally inherited mtDNA would not. It may
be that unidirectional backcrossing to males has homogenized the nuclear genome
over time to resemble one species.
Stoles (1994) undertook a preliminary study of 10 allozyme loci for 10 indi-
viduals from the two divergent S. australasicus lineages. No differences were
noted between the nuclear genes in these two lineages. Thus it appears that the
mtDNA of one species has introgressed into the other, while the nuclear genome
regained its original state presumably through backcrossing. However, more in-
tensive analysis of nuclear genes could recover bits of genetic evidence proving
hybridization, particularly in the clade of individuals containing a mixture of
mtDNA lineages. Additional nuclear markers applied to both S. australasicus and
S.japonicus might better resolve this question.
Stoles et al. (1998) noted a divergence between Pacific and Atlantic popula-
tions of S.japonicus. Restriction enzyme analysis of mtDNA molecules from 246
S.japonicus and S. australasicus (Stoles et al., 1998, Figure 3) showed a division
of Pacific and Atlantic S.japonicus within the clade containing both species. The
geographic sorting of the two japonicus lineages by ocean basin suggests that
these might represent separate species. There is some weak morphological evi-
dence for this as Pacific populations are unmarked or only slightly marked on the
belly compared to the strong markings present in the Atlantic populations (Matsui,
1967, Table 7). In addition, the mandibular and premaxillary teeth are only lightly
crenulated in Pacific populations versus strongly crenulated in Atlantic popula-
tions. Given this evidence, Collette (1999) decided to recognize the Atlantic pop-
ulations as a separate species, Scomber colias.
III. CONCLUSIONS
This chapter demonstrates the value of examining both morphological and

molecular data in constructing hypotheses about the evolution of scombrid fishes.
Each data set provides directions as well as areas of focus for the other. Scombrid
fishes have a rich history and morphological systematists have identified numer-
ous morphological and physiological characters. However, they still have not un-
raveled the evolutionary history. More data are required in some cases to tease
apart the true relationships (e.g., Gusterochisma). However, in several cases the
evolutionary history of the group was clarified by examining the molecular data.
For example, the morphological controversy surrounding the placement of
Acanthocybium was put to rest. In another case, molecular data showed that the
subgenus Thunnus was not monophyletic since bigeye (1: obesus) clustered
weakly with the tropical Neothunnus and not its hypothesized Thunnus relatives.
The morphological data likewise indicated that the bigeye tuna appeared to be
intermediate between Neothunnus and Thunnus. On occasion molecular data have
provided reason for reexamining morphological hypotheses. For example, all the
molecular data indicate the albacore is the most divergent lineage of Thunnus. Few
have examined the evolution of the Thunnus lineage in this light (Block et al.,
1997). Future investigations should seek to clarify which is the most primitive
member of the genus as it has tremendous bearing on theories of the evolution of

endothermy of tunas.
The evolutionary history of the Scombridae is among the most interesting to
examine in bony fish. Endothermy, along with the unique form of swimming
known as “thunniform,” arose with numerous physiological and morphological
characters that have evolved only in this lineage. Until we fully understand the
evolutionary relationships we will not be able to comprehend the direction of
character evolution for either complex trait. We advocate examining both types of
data and trying to understand differences between trees based on molecules and
morphology. Combining data into “total evidence” trees where morphology and
molecules are put into a single data matrix to draw a tree might provide new
directions. Or the use of alternative molecular markers and analysis may finally
clarify some of the deeper nodes in the tree where apparent rapid speciation events
may be confusing the tree topology. Some molecular markers, particularly those
that identify insertion or deletion events of multiple nucleotides along a segment
of DNA or those that analyze DNA structure beyond the typical primary sequence
structure, have proven useful in the systematics of other difficult taxa. These mark-
ers include secondary structures of ribosomal genes (Reeb, 1995; Billoud et al.,
2000) and repetitive sequences scattered in the genome such as short interspersed
nuclear elements (e.g., Shedlock and Okada, 2000). To date, no one has used these
approaches for scombroid phylogeny.
One of the most fascinating evolutionary questions surrounding the scombrid
fishes centers upon understanding how and why endothermy evolved. Whether this
occurred in warm or cold seasremains an open question. The inability of molecular
data to unequivocally resolve the position of Allothunnus does not negate the im-
portance of the recent discoveries of countercurrent heat exchangers (Graham and
Dickson, 2000). Both data sets agree thatAlZothunnus is apart of theThunnini-Sar-
dini continuum. The exact placement of this fish within the continuum based on mo-
lecular data requires further investigation. Allothunnus shares several derived fea-
tures with the Thunnini which would corroborate its morphological placement as
sister taxa to more derived tuna lineages. The existence of this fish in cool southern
oceans would suggest that the endothermic condition and the concomitant benefits
of muscle tissue warming began in a cold-water temperate fish. Supporting this hy-
pothesis would be the independent evolution within the scombrid fish of the heater
organs in the cold-water Gasterochisma. Complications in the hypothesis arise
when examining Au&, Euthynnus, Katsuwonus, and Thunnus due to the lack of
agreement on the exact evolutionary relationships within the genus Thunnus. Fu-
ture efforts should be directed at finding additional characters, either genetic, mor-
phological, or physiological (e.g., some Thunnus such as the yellowfin have coun-
tercurrent blood supply within the cecum tissue), for analysis. Once the systematics
is clarified, a greater understanding of evolutionary change among these unusual,
widespread, commercially exploited species will be obtained.
ACKNOWLEDGMENTS
Helpful comments on drafts of the manuscript for this chapter were provided by Drs. Kent
Carpenter, G. David Johnson, and Michael Vecchione. We thank Seinen Chow for access to unpub-
lished data.
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1. SYSTEMATICS OF THE TUNAS AND MACKERFLS 33
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2
TUNA METABOLISM AND ENERGETICS

KEITH E. KORSMEYER
HEIDI DE WAR
I. Introduction
II. History of Tuna Metabolic Studies
III. Metabolic Rates
A. Standard and Routine Metabolic Rate
B. Maximum Metabolic Rate
C. Scaling of Metabolic Rate
D. Temperature Effects on Metabolic Rate
E. Hypoxia Effects on Metabolic Rate
F. Metabolic Rate and Swimming Velocity
IV. Oxygen Uptake and Delivery
V. Metabolic Capacity of Tissues
A. Red Muscle
B. White Muscle
C. Other Tissues
VI. Multiple Metabolic Demands
A. Specific Dynamic Action (Ri.1
B. Growth and Reproduction (R,,,)
C. Oxygen Debt Recovery (R,)
D. Modeling Multiple Metabolic Costs
VII. Discussion and Conclusions
A. How Does the Metabolic Rate of Tunas Compare with Other Fishes?
B. What Are the Adaptations Related to Supporting the Energetic Demands of Swimming and
Other Metabolic Processes?
C. How Do Tuna Energetics Relate to Their Swimming Performance’?
D. What Metabolic Processes Account for the Total Energetic Costs in Tunas?
E. Finally, How Does the Metabolism of Tunas Relate to Their Pelagic Existence and the
Evolution of Regional Endothermy?
VIII. The Future
Reports of the tuna’s extreme swimming capabilities and endothermy have

resulted in considerable interest in their metabolism. Progress in tuna energetics
has been linked to the development of methods and facilities for their study as
35
Tuna Volume 19 Cupynght 0 2001 by Academx Press
FISH PHYSIOLOGY All ngbts of reproduction m any form reaerved.
36 KEITH E. KORSMEYER AND HEIDI DEWAR
well as the newly available data for closely related species and other active tele-
osts. Metabolic measurements indicate that, although standard metabolic rate
(SMR) is elevated in tunas compared with many species, similar SMR and routine
metabolic rates are observed in other active fish. The elevated SMR is associated
with an increase in aerobic scope, which reduces potential energetic limitations
on physiological functions. Consequently, tuna can meet their basal metabolic de-
mands (SMR and locomotion) without compromising recovery from oxygen debt,
digestion, growth, or reproduction. Contrary to previous reports, tunas appear to
be no more efficient swimmers than other teleosts, at least during steady, sustained
swimming in a swim tunnel. High metabolic rates require that all steps in the path
from the gills to the mitochondria facilitate high levels of oxygen and metabolite
flux. While some differences exist between tunas and other active fishes at the
gills, cardiovascular system, and tissue, the most marked difference, other than
endothermy, is that the total aerobic capacity of the white muscle tissue mass is
greater than that of the red muscle. The white muscle’s aerobic capacity facilitates
rapid recovery from oxygen debt incurred during burst swimming. Studies com-
paring the tuna with ectothermic scombrids suggest that endothermy may have
evolved following an increase in aerobic poise.
I. INTRODUCTION
Tunas, with their sleek bodies, warm muscles, and powerful swimming, are
the focus of considerable interest, particularly in the areas of metabolism and en-
ergetics. How do these predatory fish grow so rapidly and swim so quickly, ap-
parently expending large amounts of energy, while living in a pelagic ocean en-
vironment which is generally depauperate of prey (Blackburn, 1968)? Tunas, like
other animals, use chemical energy acquired from prey to perform the various
functions of life. The amount of energy acquired must exceed the amount ex-
pended by daily activities to permit growth and reproduction. Based on optimal
foraging theory, natural selection should operate to maximize the ratio of energy
income to energy expenditure (Webb, 1975; Townsend and Winfield, 1985). The
more efficient individuals, at a given energy intake, will have more energy to in-
vest in growth and reproduction, and therefore have a higher fitness. How do tunas
fit into this scheme? This question not only has implications for energetics but
may also provide insight into the evolution of endothermy.
Much of the research on tunas over the last 30 years has focused on measuring
metabolic rates, in attempt to quantify swimming costs, and to ascertain the conse-
quence of endothermy on metabolic function (Stevens, 1972; Brill, 1979, 1987;
Gooding et al., 1981; Graham et al., 1989; Boggs and Kitchell, 1991; Dewar and
Graham, 1994). Measured metabolic rates of tunas exceed those of other well-stud-
ied fishes (e.g., salmonids) by approximately threefold. These observations have
2. TUNA METABOLISM AND ENERGETICS 37
led to investigations into the adaptations enabling high rates of oxygen uptake, de-
livery, and utilization as well as how energy is partitioned (Muir and Hughes, 1969;
Brill and Bushnell, 1991; Mathieu-Costello et al., 1992; Moyes et al., 1992; Dick-
son, 1995; Freund 1999). The purpose of the present review is to highlight the ad-
vances in tuna energetics, and draw some conclusions about the possible implica-
tions for the questions raised above. Specifically, how does the metabolic rate of
tunas compare with other fishes? What are the adaptations related to supporting the
energetic demands of swimming and other metabolic processes? How do tuna en-
ergetics relate to their swimming performance? What metabolic processes account
for the total energetic costs in tunas? Finally, how does the metabolism of tunas re-
late to their pelagic existence and the evolution of regional endothermy?
A great deal of new information has been gained since the last major review of
tuna physiology (see The Physiological Ecology of Tunas, Academic Press, 1978).
Much of our recently gained knowledge of tuna biology has benefited from greater
emphasis on appropriate phylogenetic comparisons. Only by using the comparative
approach can we sort out those features of tunas which are the result of adaptation
to the pelagic environment or the acquisition of endothermy, and which are due to
evolutionary constraints (Block and Finnerty, 1994). Historically, tunas have been
distinguished by comparison with salmonids (Gooding et al., 1981; Dewar and
Graham, 1994), which provide the largest experimental data base in fish biology.
Salmonids, however, are both distantly related to tunas (by approximately 100 mil-
lion years of evolution; Carroll, 1988) and have a markedly different ecology (as
anadromous or freshwater fishes from temperate and polar regions, whereas most of
the physiological data on tunas come from studies of tropical species). Recent ef-
forts have provided data on close relatives within the family Scombridae, which in-
cludes the mackerels (tribe Scombrini), seerhshes (tribe Scomberomorini), bonitos
(tribe Sardini), and tunas (tribe Thunnini), and other large, warm-water pelagic fish.
such as the dolphinfish (family Coryphaenidae; Benetti etal., 1995; Dickson, 1995,
1996; Freund, 1999). Comparisons with the ectothermic scombrids, such as the
mackerel and bonito, are of particular importance in examining the interplay be-
tween endothermy and energetics.
II. HISTORY OF TUNA METABOLIC STUDIES
To understand the current state of the field of tuna energetics it is useful to

examine the historical developments that have driven its progress. Tuna research
on metabolic rates has lagged far behind that of salmonids, which was relatively
advanced by the early 1970s (Brett, 1964, 1965; Beamish, 1970; Brett and Glass,
1973; Webb, 197 1; summarized in Webb, 1975). Efforts to study tunas have been
hampered by the inherent difficulties in handling these large, active, pelagic fish.
As a result, progress in the field has been tied to the advancement of new tech-
niques. Of critical importance has been the ability to maintain animals in captivity.
Most research on live tunas (primarily the skipjack tuna Kutsuwonuspelamis, yel-
lowfin tuna Thunnus albacares, and kawakawa Euthynnus afinis) has been con-
ducted on small fish (0.5 to 5 kg) at the National Marine Fisheries Service, Kewalo
Research Facility, in Honolulu, Hawaii (Brill, 1992; Nakamura, 1972). More re-
cently, the Tuna Research and Conservation Center in Monterey, California (Al-
tringham and Block, 1997; Dewar et al., 1999), has provided access to larger fish
and also expanded the species held to bluefin tuna (Thunnus thynnus). Another
important step was the development of a large recirculating water tunnel, which
allowed physiological studies where swimming speed and environmental condi-
tions could be controlled (Graham and Laurs, 1982; Graham et al., 1989). Given
the focus on locomotory abilities, quantifying physiological variables as a func-
tion of swimming speed was critical.
Over the last 30 years, researchers have used a variety of techniques in at-
tempting to quantify the metabolic rates of tuna. Efforts began with measurements
of the oxygen consumption of minced slow- and fast-twitch muscle tissue taken
from skipjack and bigeye tuna (Thunnus obesus; Gordon, 1968). Interestingly, tis-
sue metabolism changed little with temperature (Qlo, the factor by which the rate
changes with a 10°C increase in temperature, of l-l .2) and values for skipjack tuna
aerobic, slow-twitch muscle (hereafter termed red muscle) were similar to mam-
malian muscle at 30 and 35°C. The applicability of these measures to in vivo con-
tracting muscle is not clear. Stevens (1972) was the first to estimate whole-body
metabolic rates by measuring the fraction of oxygen removed from water passed
over the gills of an anesthetized tuna. Results from this study suggested that the
metabolic rate of tuna (692 mg 0, kg -I h-l) was at least four times higher than that
of rainbow trout (Oncorhynchus mykiss). Brill(l979,1987) obtained a more direct
measure of metabolic rate by recording whole-animal rates of oxygen consumption
from immobilized tropical tunas. These results (detailed below) provided estimates
of the minimal metabolic demands, as well as effects of body size and temperature,
and confirmed the assertion that metabolic rates in tuna were elevated.
The first measurements of oxygen consumption by swimming tuna were made
by Gooding et al. (1981) on small groups of captive or recently captured skipjack
tuna. The fish swam in an annular tank respirometer where swimming speed was
estimated by averaging lap times for the group, providing the first estimate of
velocity effects. These results were complicated by the determination of group
averages rather than values for individual fish and the inability to precisely deter-
mine velocity. Also, the use of recently caught fish may overestimate metabolic
rates due to anaerobic debt incurred during capture (Dewar and Graham, 1994)
and digestive processes in postprandial fish. Using a different approach, Boggs
(1984; Boggs and Kitchell, 1991) estimated metabolic demands by measuring
reductions in caloric density of body tissues during fasting in captive groups of
tuna. Despite the limitation of each technique and their differences, estimates of
metabolic rates by Boggs were similar to those of Gooding et al. (1981).
Continued advancement in tuna energetics required the ability to monitor and

control swimming speed and temperature while oxygen consumption was re-
corded. This was made possible by the development of a large recirculating water
tunnel by Jeffrey Graham at Scripps Institution of Oceanography (Graham et al.,
1989, 1990; Graham and Laurs, 1982). The water tunnel was first used in a num-
ber of trips to sea to study albacore tuna (Thrmnus aldunga; Graham and Laurs,
1982; Graham et al., 1989), providing the first metabolic measurements made at
controlled velocities. Graham then moved the water tunnel to the Kewalo Re-
search Facility in Hawaii in the early 199Os, where captive-acclimated fish could
be studied while swimming for up to 31 hours. Dewar and Graham (1994) were
able to examine the influence of temperature, size, and swimming speed on the
metabolic rate of yellowfin, kawakawa, and skipjack tunas.
While much has been done to define the metabolic parameters of a few tuna
species, our ability to interpret these data has been limited by the lack of appro-
priate comparisons. In recent years, however, a number of researchers have been
focusing on comparable measures for ectothermic scombrids, as well as other ac-
tive tropical fish species (Benetti et al., 1995; Dickson, 1995; Freund, 1999; Se-
pulveda and Dickson, 2000). Freund (1999), using the methods of Gooding et al.
(198 l), measured the routine metabolic rates the bonito, in comparison with skip-
jack and yellowfin. Sepulveda and Dickson (2000) have compared the metabolic
rates of similarly sized tuna and mackerel swimming in a water tunnel. These
phylogenetically correct comparisons improve our ability to determine the func-
tional significance of the tuna’s adaptations.
III. METABOLIC BATES
A number of different metabolic levels, or states, have been identified which

facilitate comparisons among different studies and species. Standard metabolic
rate (SMR) is defined as the resting and fasting metabolism at a given temperature.
This is theoretically the minimal metabolic rate of the animal. The aerobic me-
tabolism during low levels of spontaneous activity is termed the routine metabolic
rate (RMR) and may cover a wide range of values depending on conditions. Fi-
nally, we can identify the maximal rate of aerobic metabolism (MMR).’ The dif-
ference between MMR and SMR indicates the animal’s aerobic metabolic scope
available to power activities (Fry, I97 1). The above metabolic designations do not
‘We have chosen to use this MMR designation rather than the more traditional “active metabolic
rate,” or AMR, for several reasons. Active metabolic rate has been used to identify the maximal
aerobic metabolic rate achieved during intense, but steady, swimming (Fry, 1971; Brett and Groves,
1979), but it has also been used to identify metabolic rates associated with swimming at any velocity
(Videler, 1993). More importantly, it assumes that the maximal aerobic metabolic rate of the fish
occurs as a result of locomotor activity alone. Akhough this may be the case for many fish, it does not
hold true for all (Goolish, 1991). and may not hold true for tunas (Korsmeyer et al., 1996a).
take into account activities powered by anaerobic metabolism. Anaerobic energy

production may occur in addition to any aerobic metabolic rate and can tempo-
rarily exceed the MMR (by up to 10 times), resulting in the build up of an oxygen
debt which must be repaid later (Brett, 1972).
Most studies on tunas have used oxygen consumption (respirometry) as an
indirect measure of metabolic rate (Stevens, 1972; Gooding et al., 1981; Brill
1979, 1987; Graham and Laurs, 1982; Graham et al., 1989; Dewar and Graham
1994). While ideally one would use direct calorimetry (heat production), oxygen
consumption is relatively easy to measure and can provide information on rapid
changes (on the order of minutes) in metabolic demands, and errors associated
with the difference in energy released by oxidation of different metabolic sub-
strates is minimal (Randall et al., 1997). Respirometry is limited, however, in that
it cannot detect anaerobic contributions to metabolism. Also, comparisons be-
tween studies are sometimes complicated by the different metabolic states mea-
sured as well as the influence of stress, feeding, body mass, and temperature.
Despite these problems, sufficient data are available to make some general conclu-
sions about how tunas compare with other fishes.
A. Standard and Routine Metabolic Rate
Tunas must swim continually to maintain ventilatory water flow and generate
sufficient lift to prevent sinking and thus never achieve the “resting state” which
defines SMR (Magnuson, 1978). Estimates of SMR, however, are valuable as a
basis for comparison with other species and for determining how resources are
partitioned. For fish which swim continually, SMR is estimated using two meth-
ods: oxygen consumption (&LO,) of immobilized specimens (by neuromuscular or
spinal block), and extrapolation of MO, and swimming velocity relationships
back to zero swimming speed (Brill, 1979, 1987; Gooding et al., 1981; Graham
et al., 1989; Dewar and Graham, 1994). Both methods have been validated in
other fish species and provide similar results (Brett, 1964; Bushnell et al., 1984;
Brill, 1987; Dewar and Graham, 1994).
Standard metabolic rate data for tunas, with comparisons to other fish species,
are summarized in Figure 1. The nontuna species chosen for comparison are con-
sidered to be active swimmers which generally have higher SMRs than more slug-
gish, or bottom-dwelling, species (Brett, 1965; Brett and Groves, 1979). The
SMRs for tunas are 2 to 10 times greater than those for most active fishes shown
in Figure 1, even when differences in temperature are taken into account. How-
ever, SMRs of some active pelagic fishes, such as dolphinfishes (Coryphaenu hip-
purrs), are similar to those of tunas (Figure 1; Benetti et al., 1995). Like the tunas,
dolphinfish are obligate ram ventilators, have large gill surface areas, and have
high growth and reproductive rates (Palko et al., 1982; Benetti et al., 1995; Brill,
1996). Another active pelagic fish, the yellowtail (Seriolu quinquerudiata, family
albzcore 15 “C 4
yellowfin 24 “C ’
k A f7L-- yellowtait 20 “C ”
/
/
L sockeye salmon 20 “C ”
/
nackerel24 ‘C9-W~
mackerel 15 “C ”
. ..( . . , . . . ,
0.1 1 10
Body Mass (kg)

Fig. 1. Standard metabolic rate (mg 0, h. ‘) as a function of body mass (M, kg) for tunas (solid
symbols, solid lines) compared with other active fishes (open symbols, dashed lines). ‘Karsuwonus
pehmis; SMR = 412.0 IV”~~’ (Brill. 1979). 2Eurhynnus afinis; SMR = 392.5 M”4y6 (Brill. 1987).
‘Thunnus albacares; SMR = 286.8 M or71 (Briil, 1987). AThunnus alulunga (Graham et al., 1989).
5Thunnus albacares (Dewar and Graham, 1994). 6Thunnus albacares, ‘Euthynnus a&is, and sScom-
ber japonicus calculated from data in Sepulveda and Dickson (2000) by extrapolating the logarithm
of oxygen consumption as a function of velocity to zero velocity. ‘Coryphaena hippurus (Benitti et al.,
1995). “‘Oncorhynchus nerka (Brett and Glass, 1973). “Oncorhynchus nerka from Brett and Glass
(1973) corrected to a temperature of 25°C assuming Q10 = 2. ‘20ncorhynchus mykiss (Bushnell et al.,
1984; Brill, 1987). “Brevoortia tyrannus (Macy et al., 1999). 14Trachurus trachurus (Wardle et al..
1996). 15Dicentrarchus 1abru.x (Herskin and Steffensen, 1998). ‘“Sconberjaponicus (Steffensen and
Shadwick, unpublished data). “Kuhlia ~andvicrnsis (Brill, 1987). iXSrriola quinquerudiutu (Yama-
moto er al., 1981).
Carangidae), has an SMR intermediate between those of tunas and other fishes
(Figure 1; Yamamoto et nl., 198 1). Correcting for temperature differences, the
tunas have SMRs that are only 1.4 to 2.0 times that of the yellowtail. Within the
family Scombridae, SMR values are available only for the Pacific mackerel
(Scomber juponicus). Similarly sized yellowfin and kawakawa, at the same tem-
perature, have SMRs that are about 4 times greater than that of the mackerel (Fig-
ure 1; Sepulveda and Dickson, 2000).
Unlike the mackerel, another scombrid, the eastern Pacific bonito (&~-da chi-
liensis), appears to have similar metabolic rates as the tunas’. RMRs of the bonito
and skipjack tuna were recently compared while the fish swam in an annular res-
pirometer (Freund, 1999). The &IO, values of skipjack (540 t 63 mg 0, kg-’ h-l)
and bonito (427 It 63 mg 0, kg-’ h-l), which had similar masses (- 1.4 kg) and
average swimming velocities [OS lengths (L) s-l, measured by recording lap
times], were not significantly different.
The picture that is emerging is that while tunas have higher metabolic rates
than many active fishes, including mackerel, so do some other pelagic species
(e.g., dolphinfish and bonito). Therefore, fishes can have a high metabolic rate
without the elevated tissue temperatures associated with endothermy.
B . Maximum Metabolic Rate
Maximum metabolic rate has not been measured directly in tunas, ectothermic
scombrids, or other tropical pelagic fishes. A few very high &IO, values have been
measured for tropical tunas (23-25”C), but whether these represent a maximum
is not known. The mean &IO, measured for groups of skipjack tuna within the first
two hours after capture at sea was 1300 mg 0, kg-’ h-’ (1.8-2.2 kg body mass;
Gooding et al., 1981). Individual measurements ranged from 900 mg 0, kg-l h-l
to the highest &IO, ever recorded for fish of this size, 2500 mg O2 kg-’ h-l. These
fish were swimming at high speeds (-3.5 L s-l), were likely recovering from
anaerobic activity, and may have been digesting food. A similarly high hilO, was
recorded for one skipjack just after it was placed in a swimming respirometer
(2200 mg 0, kg-’ h-l, - 1.7 kg; Dewar and Graham, 1994). The highest recorded
&IO, for yellowfin in a swimming respirometer was 1290 mg 0, kg-’ h-l (-2 kg;
Dewar and Graham, 1994). While these values may be less than the MMR, they
do provide an estimate for its lower limit.
With the lack of any clear data, models have been developed to predict MMRs
for tunas. Expanding on a model by Dizon (1977), Bushnell and Brill(l991; Brill,
1996) calculated maximum rates of oxygen extraction from the ventilatory water
flow in yellowfin and skipjack tunas as a function of swimming speed. Maximum
oxygen uptake for a body mass of 1.4 kg was predicted to be 2500 mg 0, kg-’
h-’ for yellowfin and 2700 mg 0, kg-’ h-l for skipjack (Bushnell and Brill, 1991).
For 2.0-kg fish, the MMR is predicted to be 1600 and 1800 mg 0, kg-l h-l for
yellowfin and skipjack, respectively (Brill, 1996). These model values of MMRs
are considerably higher than the upper limit of hi0, reported for a number of other
fishes (-1000 mg O2 kg-’ h-l; Brett, 1972).
One impetus for documenting MMRs is to calculate the aerobic scope, which
would indicate the level of aerobic activity that can be sustained. Based on the
values discussed above, a 2-kg skipjack (SMR - 300 mg 0, kg-’ h-l; Brill, 1979)
should have an aerobic scope of between 1500 and 2200 mg 0, kg-’ h-‘. This is
considerably higher than that for a comparably sized sockeye salmon at approxi-
mately 700 mg 0, kg-’ h-l (20°C; Brett and Glass, 1973). Interestingly, the esti-
mated ratio of MMR to SMR for tunas (6-10) is similar to that of both other active
fish species and terrestrial vertebrates (Brett and Groves, 1979; Bennett and
Ruben, 1979; Else and Hulbert, I981,1985). It seems that the high SMRs of tunas
are associated with a very high aerobic scope. Actual measurements of MMR in
tunas and other pelagic fishes are needed to verify this.
C. Scaling of Metabolic Rate
SMR data for tunas over a significant size range (Figure 1) allow for estima-
tion of the effect of body size on metabolic rate. Because of the difficulty of work-
ing with large fish, however, data are only available for relatively small body
masses (0.1 to 10 kg). Given that yellowfin and bluefin tuna can grow as large as
180 and 680 kg, respectively (Collette and Nauen, 1983), extreme caution should
be used in extrapolating these data much beyond 10 kg body mass.
The effect of body size can be described by the allometric equation relating
metabolic rate and body mass (M),
SMR = aMh.
where a (intercept) and b (slope) are constants. Brill(l979, 1987) calculated mass
exponents (b) of 0.50 for kawakawa (0.5-2.2 kg), 0.57 for yellowfin (0.6-3.9 kg),
and 0.56 for skipjack (0.3 - 4.7 kg), based on MO, in spinally blocked fish. Dewar
and Graham (1994) reported similar results (b = 0.60, 0.5-2.2 kg) for SMRs
determined by extrapolating the yellowfin MO, as a function of velocity to zero
velocity. The SMRs of much smaller (-0. l-kg yellowfin and kawakawa) and
larger tuna (-lo-kg albacore) fit very well with the predicted MO2 based on these
mass exponents (Figure 1; Graham et al., 1989; Sepulveda and Dickson, 2000). A
few earlier studies reported scaling of greater than unity for tunas [b = 1.18, mass
range 0.6-3.8 kg (Gooding et al., 1981); b = 1.19, mass range 8.5-12 kg (Gra-
ham and Laurs, 1982)]. However, these estimates likely result from basing com-
parisons on RMRs (i.e., the MO, of swimming fish) rather than SMRs.
Tunas appear to have lower scaling exponents (0.5 to 0.6) compared with other
fishes (range 0.65 to 0.9, average -0.80; Jobling, 1994; Clarke and Johnston,
1999) and most animals (average -0.75; Randall et al., 1997). This difference
indicates that mass-specific SMR in tunas decreases relatively rapidly as body
mass increases (Brill, 1987). Given that the basis for SMR is poorly established,
the reasons for this are difficult to interpret. Interestingly, Graham et al. (1983)
found that the exponents for the scaling of red muscle mass with body mass were
less than 1 in tunas (0.66-0.96), and greater than 1 in other scombrids (1.23-
1.72). In other words, the relative amount of red muscle mass as a proportion of
total mass decreases in larger tunas. If maintenance of the highly metabolically
active red muscle contributes to SMR, this may partially explain the lower scaling
exponent. It has been suggested that osmoregulatory costs are a large component
of SMR (Brill, 1987). Thus, one might expect the scaling relationship of gill sur-
face area, the site of most osmoregulatory exchange, and SMR to be closely
matched. However, the scaling relationship determined for total gill area in tunas
is 0.85, which is similar to other fishes (Muir and Hughes, 1969; Hughes, 1984).
Others have suggested that total gill area likely limits maximal rates of oxygen
uptake, and therefore it should scale with MMR, rather than SMR (Hughes, 1984).
This difference in gill area and SMR scaling suggests that larger tunas may have
a greater aerobic scope than smaller tunas (Brill, 1987). Clearly additional mea-
sures, such as osmoregulatory costs, mitochondrial characteristics, and the main-
tenance of the different tissues and organ systems, need to be examined over a
range of sizes. This information will be especially critical if we hope to make
inferences about the SMR of larger tunas.
D. Temperature Effects on Metabolic Rate
Tunas regularly experience large (- 10” C) changes in temperature as a result

of both vertical and horizontal movements in the ocean (Holland et al., 1990; Brill
et al., 1999; Gunn and Block, this volume). Acute temperature effects have been
examined in tunas for both SMR and swimming &IO,, and indicate a similar re-
sponse in tunas, most teleosts, and terrestrial ectotherms (Q 10= 2-3; Bennett and
Ruben, 1979; Brett, 1964; Brett and Glass, 1973; Brill, 1987; Dewar and Graham,
1994; Clarke and Johnston, 1999). Brill(1987) measured the change in SMR with
temperature of tuna paralyzed with a neuromuscular blocking agent. The QlO’s
calculated over the range of 20 to 25°C were 2.44 for skipjack, 3.16 for kawakawa,
and 2.3 1 for yellowfin. Examination of temperature effects on swimming tuna is
complicated by their ability to elevate and control muscle temperature (Carey
et al., 1971; Dewar et al., 1994). At a given ambient temperature, muscle tempera-
ture may differ depending on thermal history and swimming speed (and therefore
muscle heat production). Dewar and Graham (1994) measured a Q10 of 1.67 for
swimming yellowfin by changing temperature (18-30°C) while maintaining a
constant speed. The lower Q ,” in swimming tunas, compared with nonswimming
subjects, could have been a result of their ability to increase excess muscle tem-
peratures in cooler water. However, despite regional endothermy, tuna metabolic
rates are still directly related to ambient temperature, which may limit tuna distri-
butions and swimming performance (Brill, 1994; Korsmeyer et al., 1996b; Brill
et al., 1999).
E. Hypoxia Effects on Metabolic Rate
In many areas, tunas may come into contact with waters of low oxygen con-
tent, which, like temperature, potentially limits their movements and distributions
(Brill, 1994). Skipjack, yellowfin, and bigeye respond behaviorally (increases in
swimming speed) and/or physiologically (increases in ventilation volume and de-

creases in heart rate) to moderate hypoxia between ambient oxygen partial pres-
sures (PO,‘s) of 17.3 and 12.0 kPa (about 80 to 60% saturation; Dizon, 1977;
Gooding et al., 1981; Bushnell et al., 1990; Bushnell and Brill, 1991, 1992; Kors-
meyer, 1996; Korsmeyer et al., 1996b). Bushnell and Brill ( 1992) determined that
a PO, of 12.0 kPa limited oxygen delivery by the cardiorespiratory system in spi-
nally blocked skipjack. This is caused by a hypoxia-induced decline in heart rate
(bradycardia) which lowers cardiac output (see Brill and Bushnell, this volume).
Yellowfin were more hypoxia tolerant, with limitation occurring at 6.7 kPa 02,
although Dizon (1977) found they could survive severe hypoxia (4.0 kPa) for
greater than 200 min. Experiments by Graham et al. (1989) showed that the swim-
ming ti0, of albacore (0.5 -I .4 L s. ‘) exposed to moderate hypoxia (between 6.7
and 13.2 kPa 02, 15°C) was lower than rates in normoxia, suggesting an inability
to maintain oxygen delivery within this range.
As tunas are ram ventilators. they may depend on increasing swimming speed
in hypoxia in order to maintain oxygen supply to the gills. An increased swim-
ming speed has been seen in both skipjack and yellowfin in response to hypoxia
(Dizon, 1977; Gooding et al., 198 1; Bushnell and Brill, 199 1). However, increases
in swimming velocity will increase oxygen demand, and it is thus a somewhat
paradoxical response to hypoxia. It may be that the velocity increase is an attempt
to leave the area of hypoxia rather than compensation for these conditions (Dizon,
1977; Bushnell and Brill, 199 1).
F. Metabolic Rate and Swimming Velocity
Much of the attention on tunas has resulted from their reported high-speed
swimming abilities. Tunas traverse large distances during oceanic migrations and
are clearly capable of rapid accelerations in short-duration swimming bursts
(Mather, 1962; Magnuson, 1978; Walters and Fierstine, 1964; Fierstine and Wal-
ters, 1968). All tunas elevate the temperature of their swimming musculature with
a presumed increase in muscle performance (see Altringham, this volume). Also,
much of their external morphology would appear to increase swimming efficiency
through reductions in drag, and consequently costs of locomotion (Webb, 1975;
Magnuson, 1978; Dewar and Graham, 1994). To define the energetic implications
of the these adaptations requires that the relationship between h;lO, and velocity
(U) be defined.
The relationships between h;IO, and U measured for a number of tunas are
shown in Figure 2. Among respirometry studies, the logarithm of ti0, is propor-
tional to velocity, and the rate of increase is similar for yellowfin (Dewar and
Graham, 1994), skipjack (Gooding et al., 1981), and albacore tunas (Graham
et al., 1989). The lower mass-specific h;IO, of albacore is expected given their
greater mass (8.5-12 kg) and the lower water temperature (- 15°C) than in the
skipjack2
, skipjack3 0
.g 600
8 500
B
8 400
300 yellowfin
I ‘I’, / I ” I”, / ” /’
0.00 0 25 0.50 0.75 1.00 1.25 1.50 1.75
Velocity (m s-l)
Fig. 2. Metabolic rate (&IO,, mg 0, kg’h- ‘) as a function of swimming speed (U, m s-l) for
skipjack (Kutsuwonus pelamis) and yellowfin tuna (Thunnus albucares) at 25°C and albacore (Thun-
nus alalunga) at 15“C. ‘Graham et al. (1989), ZGooding et al. (1981), ‘Boggs (1984), and 4Dewar and
Graham (1994). Estimates of metabolic rate were determined using respirometryl,z,4 and by measuring
reductions in caloric density of body tissues during fasting.’ Semilog equations for each data set are
albacore,’ log hilO, = 0.3OU + 2.39; skipjack,2 log &IO, = 0.38U + 2.46; skipjack,3 log &IO, =
1.06U + 2.05; yellowfin,’ log hi0, = 0.99U + 2.04; and yellowfin, log &IO, = 0.42U + 2.42.
other studies (-2 kg and 25°C). Boggs’ (1984) data based on changes in tissue
caloric density during starvation differ from respirometry studies (Figure 2).
Boggs’ study measured lower metabolic rates at low speeds for yellowfin, and
higher values at high speeds for both skipjack and yellowfin. This difference may
be in part due to an overestimate at slower speeds in the swimming respirometer
studies due to stress. However, in Boggs’ study of velocity effects, the relation to
metabolic rate may be confounded by the concurrent declines in swimming speed
and body mass as starvation proceeded, as well as acclimation to captivity.
The relationship between h;IO, and velocity, in comparison to similar studies
with nontunas, allows us to determine if regional endothermy in tunas, and the
features that result in thunniform swimming, results in greater swimming effi-
ciency. Previous studies have reported that tuna are more efficient swimmers than
salmonids, based on the lower slopes of the linear relationship between logarithm-
transformed h;IO, and velocity (Figure 3A; Gooding et al., 1981; Graham et al.,
2. TUNA METABOLISM AND ENEKGETICS 47
1989; Dewar and Graham, 1994). This relationship, however, is strongly depen-
dent on the intercept with zero velocity, or SMR. Increases in SMR alone will
result in a lower slope of the log-linear relationship. Removing SMR from MO,
during swimming is a measure of the metabolic increment due to locomotory
costs. Comparison of this incremental swimming cost for yellowfin tuna and simi-
larly sized (-50 cm) sockeye salmon is shown in Figure 3B. The differences be-
tween the tuna and the salmon are within the variability of the measurements,
indicating that there is no significant difference in swimming costs.
A recent study on the swimming costs of small (-0.1 kg) tunas (kawakawa
and yellowfin) in comparison with an ectothermic scombrid (Pacific mackerel)
provide further evidence that tuna have swimming efficiencies similar to other
active species (Figure 4; Sepulveda and Dickson, 2000). The two tunas have simi-
lar rates of increase in MO, with U as the mackerel (although SMRs are much
higher, as discussed above). However, we cannot make any conclusions about the
influence of endothermy on swimming efficiency based on this study. The eleva-
tion in muscle temperatures (tuna, + 1.5”C; mackerel, +0.4”C) may have been
too low for its effects to be manifested. As tuna increase in size their thermal
excess increases (Dickson, 1994), and external morphology also diverges from
that of the ectothermic scombrids (Magnuson, 1978). Consequently, similar stud-
ies comparing larger ecto- and endothermic scombrids are needed. However, at
present, there is no conclusive evidence that the energetic cost of swimming in
tunas is less than that in other fishes, contrary to previous suggestions.
In addition to determining SMR and locomotor costs, measurement of MO2 as
a function of velocity allows calculation of the cost of transport (COT). COT is
the total amount of energy expended per unit weight per unit distance (J N -.1m -‘)
at a given velocity and can be calculated from MO, using a conversion factor of
14.1 J per milligram of 0, (Tucker, 1975; Videler and Nolet, 1990; Videler, 1993).
A plot of COT versus velocity produces a U-shaped curve (Figure 3C). Where
COT reaches a minimum is defined as the optimal swimming velocity (U,,,). The
higher COT below U,,, is a consequence of the relatively large contribution of
SMR to total MO, at low speeds. As a result, Uc,ptwill be higher with increases
in SMR.
The cost of transport (COT) and optimal swimming speed (U,,) are frequently
used to characterize swimming performance. Videler (1993) compiled values of
COT at Uapt (minimum gross cost of transport, or GCOT) for a number of fishes
(most at 15°C) and other submerged swimmers. Examination of values across a
range of sizes indicates a decrease in U,,, with increasing mass (Figure 5A). Com-
paring values for similar-sized fish, the Uoptin tunas is high. For example, the Uop,
for a 50-cm yellowfin tuna is -2 L s I, compared to - 1 L s-’ for a similarly sized
sockeye salmon (Figures 3C and 5A; Dewar and Graham, 1994). This reflects the
elevated SMR observed in tunas, which increases COT at low speeds. U,, is con-
sidered a good predictor for routine swimming speeds in fishes (Videler, 1993).
yellowfin tuna 253TL--
._,/--’
--/“,-‘F”’ /
/ sockeye salmon 15 ‘C
bonito 20 ‘C /’
/
/
1’
/
I, I”,,.“,,~,.f
1 .oo 1.25 1.50 1.75
1200
1 B
yellowfin tuna 25 OC
0.00 0.25 0.50 0.75 1 .oo 1.25 1.50 1.75
yellowfin tuna 25 OC
0.75 1 .oo
Velocity (m se’)
2750 11
2500
2250
2000
1750
1500
1250
yellowfin. 111 g r-
1000
750 kawakawa. 145 g
500 _---’ -c--

250
0.0 0.1 0.2 0 3 0.4 0.5 0.6 0.7 0.8 0.9 10
Velocity (m S’)
Fig. 4. Oxygen consumption (MO,mg 0, kg ’ h ~I) versus swimming velocity (U, m s ‘) up to

the critical swimming speed in four similarly sized scombrid fishes: yellowfin tuna (Thunnus albaca-
res), a large and small kawakawa (Eufhvnnus afinis), and the Pacific mackerel (Sconzberjuponicus:
Sepulveda and Dickson, 2000). The lines are exponential curves fitted to the data. Note that the Y-
scale is linear rather than logarithmic. This is to make the actual increase in swimming costs above
SMR apparent (see text). The inset shows the same data plotted on a semilog plot, illustrating the
differences in slope that this presentation creates. The increase in MO, during swimming does not
differ significantly among species. However, at all speeds, metabolic rate is greater in the tunas than
in the Pacific mackerel, indicating that total cost and standard metabolic rate (estimated from the Y-
intercept) are greater in tunas. Semilog equations for each fish are, for mackerel, log MO* = 0.1541:
+ 2.30; large kawakawa. log MO2 = 0.07701J + 2.81; yellowtin. log MO: = 0.053OU + 2.99: and
small kawakawa. log MO, = 0.0566U + 3.02.
Fig. 3. (A) Metabolic rates (MO,: mg 0, kg~ I h ‘) as a function of swimming speed (U, m s -‘)
for a yellowfin tuna (Thunnus albacares) of 2.2 kg, 51 cm (log MO, = 0.42U + 2.4; Dewar and
Graham, 1994) and for a sockeye salmon (Oncorhynchus nerku) of I .4 kg, 54 cm (log MO, = 0.86U+
1.6; Brett, 1965). Data for salmon at 15°C are used because swimming performance was greatest at
this temperature. One value is shown for the Pacific bonito Sardu chiliensis at its spontaneous swim-
ming velocity (Freund, 1999). (B) Metabolic increment associated with swimming (MO, minus stan-
dard metabolic rate) as a function of swimming speed (m s ‘) for tuna and salmon as in A. For the
tuna, 95% confidence limits for the line’s elevation and intercept are shown. The only available error
estimates for the salmon occur at zero and the maximum velocity. For the salmon, values between the
minimum and the maximum velocity represent the lowest MO, recorded at a given speed. (C) Cost of
transport (COT; J N. ’ m-l) as a function of velocity (m s +I for the tuna and salmon as in A and B.
The optimal swimming velocity, where COT reaches a minimum. is indicated for both species.
3A yellowfin l
l skipjack
- !
02
‘0 l yellowfin
‘;
en q3
z
7 0 albacore
Es 0.1 1
8
17
i C
1
Mass (kg)
including tunas (Dewar and Graham, 1994), suggesting that fish usually swim at
speeds at which transport costs are at a minimum.
Similar to U,, GCOT decreases with increases in body mass in fishes (Vide-
ler, 1993). A larger animal needs fewer strides to cover the same absolute distance.
Body size effects can be removed by multiplying GCOT by body length; this is
the gross cost of transport per unit weight over one body length at U,, (GCOT X
L, in J N-l; Videler, 1993). Compared with other fishes, GCOT for tunas is greater
(Figure 5B). GCOT X L in tunas (mean = 0.15 J N-l, from values plotted in
Figure 5 multiplied by length) is about twice tbat of other fishes (-0.07 J N-‘;
Videler, 1993). However, this value for tunas is half that for other submerged
swimmers (GCOT X L = 0.30 J N-l for invertebrates, penguins, and marine
mammals; Videler, 1993). The elevation in GCOT in tunas relative to other fishes
is due in part to a higher U, and SMR. Removal of SMR from GCOT produces
the net cost of transport (NCOT). Even with this correction, NCOT in tunas is
greater than that of other fishes (Figure 5C). These comparisons at U,,, suggest
that swimming in tunas is actually more costly than in other fishes. However, the
tuna’s high SMR results in a higher U,, and we would expect net swimming costs
to be greater at a higher swimming velocity given the exponential increase in MO,
with increasing U.
IV. OXYGEN UPTAKE AND DELIVERY
The high metabolic rates of tunas have resulted in many investigations of the
tuna’s cardiorespiratory system, in search of specializations that permit rapid oxy-
gen delivery to the tissues. This is not to imply that the only function of these
systems is to supply oxygen, as they are also essential for metabolic substrate
delivery and waste removal (Heisler, 1989; Weber, 1992). However, one of the
most immediate requirements for high rates of aerobic metabolism is adequate 0,
delivery (Priede, 1985).
Tunas are obligate ram ventilators, relying on the forward motion of swim-
Fig. 5. (A) Optimal swimming velocity (U,,) in lengths per second (L s-I), (B) gross cost of
swimming at U,, (GCOT), and (C) net cost of swimming at U, (NCOT) related to body mass for
tunas (a), other fishes (a), and general regressions for fishes (-) as determined by Videler (1993).
Values calculated using methods of Videler and Nolet (1990) and Videler (1993). Yellowfin tuna
(Thunnus albacares) data from Dewar and Graham (1994), skipjack tuna (Kazsuwonus pelumis) from
Gooding et al. (1981), albacore tuna (Thunnus alalungu) from Graham er al. (1989), and sockeye
salmon (Oncorhynchus nerka) from Brett (1965). ‘Largemouth bass (Micropferus salmoides), *blue-
fish (Pomatomus saltatrix), Qtriped bass (Mot-one saxatilis), 4haddock (Melanogrammus aeglefinus),
51ake whitefish (Coregonus clupaafomis), and hrainbow trout (Oncorhynchus mykiss) values from
Table 2 in Videler and Nolet (1990). ‘Seabass (Dicentrurchus Iabrux) from Herskin and Steffensen
C1998).
ming to force water through the gill (Brown and Muir, 1970). Measured ventila-
tion volumes in tunas are high, ranging from 3 to 6 liters kg-l min-l (Bushnell
and Jones, 1994) compared with 0.2 to 0.5 liters kg-’ min-I in rainbow trout
(Kiceniuk and Jones, 1977; Davis and Cameron, 1971). Oxygen extraction from
this high rate of water flow is enabled by a large gill surface area and thin gill
epithelium (Hughes, 1984; Brill and Bushnell, this volume). The large, thin gills
of tunas are protected in the face of a high ventilatory water flow by additional
supporting tissue that fuses lamellae on adjacent filaments; this strengthens the
gill sieve and may aid gas transfer by reducing water velocity through the lamellar
channels (Muir and Kendall, 1968).
Delivery of oxygen from the gills to the tissues is dependent on the oxygen-
carrying capacity of the blood and rates of blood flow. Although arterial oxygen
contents in tunas are not extraordinary, their large hearts can generate high blood
pressures and cardiac outputs (see Brill and Bushnell, this volume). During mod-
erate exercise in yellowfin tuna, oxygen delivery is increased through near-equal
contributions of an increased cardiac output (due entirely to heart rate) and oxy-
gen extraction from the blood (arterial-venous oxygen content difference; Kors-
meyer et al., 1997). The uptake of oxygen at the tissue will depend on the capillary
area for exchange and the oxygen gradient established between the capillary and
the mitochondria. Most of the information available for oxygen delivery is for the
myotomal muscle.
The majority of tissue in a fish, approximately 60% (Bone 1978a; Graham
et al., 1983; Freund, 1999), is the swimming musculature, of which fish have two
primary types (Bone, 1978a; Johnston, 1981). Red (slow-twitch, oxidative) fibers
are typically located in a superficial lateral wedge between the epaxial and hypax-
ial regions of white (fast-twitch, glycolytic) fibers. The red muscle is specialized
for sustained, aerobic swimming contractions, while the white muscle has a high
anaerobic capacity for powerful, short-duration bursts of activity. In tunas, the red
muscle position is more internalized compared to ectothermic teleosts, extending
from the superficial lateral region in toward the backbone. The lateral wedge in
tunas may contain red, white, or pink (intermediate, or fast, oxidative-glycolytic)
fibers, depending on the species (Dickson, 1996; Freund, 1999). The internalized
position of the red muscle in tunas is associated with vascular countercurrent heat
exchangers (retia mirubiliu) which trap metabolic heat produced during muscle
contractions, allowing tuna to elevate red muscle temperature above ambient (Ca-
rey and Teal, 1969; see Graham and Dickson, this volume).
Capillary density in skipjack tuna red muscle (2880 mm-$ Mathieu-Costello
et uZ., 1992) is higher than values reported for many fishes (118-2672 rmn2;
Egginton and Johnston, 1983), but less than that in the anchovy (Engruulis en-
crusicolus, 6000 mmm2; Johnston, 1982). The mean number of capillaries around
each red muscle fiber in skipjack (4.75-4.97; Bone, 1978b; Mathieu-Costello
et al., 1992) is about 70% greater than that in the mackerels (Scomber spp., 2.8-
Fig. 6. Scanning electron micrograph of a cross-sectional view of a corrosion cast from skipjack
tuna (Karsuwonus plunk) red muscle. Note the dense envelope formed by capillaries. Based on fiber
dimensions, two muscle fibers (A and B) could be contained in the empty space. From Mathieu-
Costello et al. (1992) with permission.
2.98; Bone, 1978b; Mosse, 1979). Further increasing the area of the capillary-
muscle fiber interface in skipjack red muscle is the geometry of the capillaries.
The red muscle capillaries have numerous venular branches, which run perpen-
dicular to the fiber axis (Mathieu-Costello et al., 1992). These form dense clusters
called capillary manifolds, increasing capillary surface area around the muscle
fiber (Figure 6). Interestingly, capillary manifolds have also been found in the
flight muscles of birds, but it is not known if they are present in other active fishes.
The manifolds potentially increase the oxygen flux to the muscle fiber by increas-
ing the area for exchange and increasing capillary transit time (Mathieu-Costello
et al., 1992).
Although the capillary density in the white muscle of skipjack (543 mrn2;
Mathieu-Costello et aZ., 1992) is less than that of the red muscle, it is relatively
high compared with other fishes. The mean number of capillaries surrounding
each white muscle fiber in skipjack (4.8; Mathieu-Costello et al., 1992) is greater
than that in other teleosts (0.3-l .6; Mosse, 1979). However, capillarity in albacore
white muscle (1.2; Dickson, 1988) is more similar to other teleosts, including the
Australian mackerel Scomber austmlusicus ( 1.1; Masse, 1979).
In muscle, uptake of oxygen from the blood and diffusive transport within the
tissue are facilitated by an oxygen-binding molecule, myoglobin (M,; Stevens and
Carey, 1981; Stevens, 1982). Compared with other fishes, including scombrids,
tuna red and white muscle have high concentrations of M, (reviewed by Dickson,
1996; Marcinek, 2000). The concentration of Mb in the red muscle of Pacific blue-
fin (40 mg g-l) is more than twice that of Pacific bonito (15 mg g-l; Marcinek
2000). Although less than in the red muscle, the white muscle of tunas also has
relatively high M, concentrations (1-6 mg g-i; reviewed by Dickson, 1996; Mar-
cinek, 2000). Comparisons of Mb concentrations from near the skin and toward
the backbone indicate a twofold increase in Pacific bluefin, while no difference
was observed in bonito (Marcinek, 2000). Interestingly, a similar pattern was ob-
served for activity of the mitochondrial enzyme citrate synthase (CS), with 30%
greater activity in the deep white muscle of the bluefin. Whether the increase in
M, with tissue depth has roots in oxygen storage or aerobic capacity, or acts to
compensate for the increase in temperature, remains to be determined.
V. METABOLIC CAPACITY OF TISSUES
Although the features discussed above are critical for the delivery of oxygen
and metabolic substrates, ultimately the capacity for energy utilization by a tissue
will depend on its total mass, temperature, and specific metabolic capacity. In-
dexes of tissue aerobic metabolic capacity include capillarity and myoglobin con-
tents (discussed above), as well as mitochondrial volume density and in vitro ac-
tivities of key metabolic enzymes-often the mitochondrial enzyme citrate
synthase. Estimates of anaerobic metabolic capacity come from intracellular buff-
ering capacities and activities of lactate dehydrogenase (LDH), which catalyzes
the final step of anaerobic glycolysis (Torres and Somero, 1988). Most studies of
tuna tissue metabolic capacity have focused on cardiac muscle (see Brill and
Bushnell, this volume) and the swimming musculature, with little information for
other tissues.2
A. Red Muscle
Depending on species, the total mass of red muscle in tunas is similar to or

greater than that of other teleosts. The relative contribution of red muscle to total
body mass can be as low as 4% in albacore (Graham et al., 1983), or as high as
10 to 13% in black skipjack (Euthynnus lineatus), bullet (Aunis rochei), and frig-
ate tuna (Auxis hazard; Magnuson, 1973; Graham et al., 1983). Values for bigeye,
skipjack, yellowfin, and kawakawa tuna fall between these two extremes (6 -9%;
2For clarity and brevity, we focus our review of enzymatic activities on CS and LDH. These two
indicators of aerobic and anaerobic activity, respectively, are the most common enzymes studied. How-
ever, other enzymes from both aerobic and anaerobic pathways have been studied in tunas, and, in
general, they support conclusions based on CS and LDH. We refer the reader to Guppy and Hochachka
(1978), Hochachka et a[. (1978) Guppy et al. ( 1979), Moyes et al. (1992), and Dickson ( 1995) for
additional enzymatic profiles of tuna muscle.
Magnuson, 1973; Graham et al., 1983; Freund, 1999). This range of relative red
muscle mass for tunas overlaps values reported for ectothermic scombrids (2-7%,
Scomber, Sarda, and Acanthocybium spp.), blue marlin (Makaira nigricans, 5%),
yellowtail (5%), and salmonids (3-4%; Magnuson, 1973; Graham et al., 1983;
Johnston and Salamonski, 1984; Tsukamoto, 1984; Tang and Wardle, 1992; Dick-
son, 1995; Freund, 1999). Thus, inferences about differences in red muscle mass
depend strongly on the comparisons made.
Relative mitochondrial volume densities in skipjack tuna red muscle (16.4-
38%; Bone, 1978b; Hochachka et al., 1978; Hulbert et al., 1979; Mathieu-
Costello et al., 1992; Moyes et al., 1992) are within the range reported for most
other fishes (8-36%; Johnston, 1981; Johnston et al., 1998), but are less than that
in the anchovy (46%; Johnston, 1982). However, relative amounts of mitochon-
drial protein (48 mg g-l) are high in skipjack (80% higher than in the carp Cypri-
nus carpio) as a result of densely packed cristae within the mitochondria (Moyes
et al., 1992). Mitochondrial inner membrane surface area per unit mitochondrial
volume in skipjack red muscle (63-7 1 m2 cm -‘) is higher than that in other fishes
(36-50 m2 cm-3; Johnston et al., 1998) and even the skeletal muscles of birds
and mammals (20-60 rn? cm-+; Hoppeler and Lindstedt, 1985; Suarez et al.,
1991). This cristae surface density is possibly approaching the maximum for the
given space (Moyes et al., 1992). Although no data are available for cristae surface
densities in other scombrids, there are data on the specific activities of mitochon-
drial enzymes.
When compared at the same temperature, maximal in vitro specific activities
of CS are greater in the red muscle of tunas than that in billfishes or sluggish fish
species (Dickson, 1995). However, comparison with the ectothermic scombrids
(Sarda, Scomberomorus, and Scomber spp.) is not straightforward. Red muscle
CS activities are higher in some species of tunas, such as skipjack and frigate tuna
(Figure 7). When compared as a group, however, tunas have red muscle CS ac-
tivities that are not significantly different from those of ectothermic scombrids
(Figure 7; Dickson, 1996; Freund, 1999). This analysis suggests that the intrinsic
aerobic metabolic capacity of tuna red muscle tissue, while high compared with
fishes in general, is more similar to that of some other active pelagic teleosts
(Dickson, 1996).
One clear difference between the tunas and other teleosts is tunas’ ability to
elevate the temperature of the red muscle. The extent to which muscle temperature
is elevated (from less than 1°C up to 20°C) varies among species, and is influ-
enced by body mass, ambient temperature, and swimming activity (Carey and
Teal, 1969; Carey et al., 197 1; Graham, 1975; Graham and Dickson, 198 1; Dewar
et al., 1994; Dickson, 1994; Holland and Sibert, 1994). The increase in tempera-
ture will increase the aerobic capacity of the red muscle. Correcting for the differ-
ences in red muscle temperature, CS capacities in tunas are, on average, 70%
higher than those in ectothermic scombrids (Dickson, 1996).
Red Muscle
BLUEFIN TUNA (Thunnus thy
ALBACORE TUNA (Thunnus afdc

YELLOWFIN TUNA (Thunnus t+!bmm#
SKIPJACK TUNA (Katsuwonus @am&)
EIJ \CK SKIPJACK TUNA (Euthynnus /ie
FRIGATE TUNA (Auxis thazan$J
STRIPED BONITO (Sarda orientatis)
E. PACIFIC BONITO (.%&a chibnsis)

SIERRA MACKEREL (Scombefw~orous skwaj
PACIFIC MACKEREL (Scomberjapcmicus)
0 10 20 30 40 50 60 70 80
Citrate Synthase Specific Activity (U g -’ wet wt)
Fig. 7. Mean (+SE) citrate synthase (CS) specific activity [international units, or pm01 substrate
converted to product min-’ (gram wet weight of muscle tissue)-I] measured at 20°C in the red myoto-
ma1 muscle of tunas (solid bars) and ectothermic scombrid species (shaded bars). Overall, red muscle
CS activity in tunas does not differ significantly from that in ectothermic scombrids. Data from Dick-
son (1996 and unpublished observations).
Thus, while the intrinsic metabolic capacity of tuna red muscle is similar to
that of other active pelagic fishes, regional endothermy, and in some species
greater amounts of tissue, significantly elevates the aerobic capacity of the tuna’s
red swimming musculature relative to other teleosts (Dickson, 1996). Graham
et al. (1983) found a negative correlation between the relative amount of red
muscle and the total surface area of the heat exchanger among the tuna species.
This relationship suggests that species with better heat conservation (and therefore
greater red muscle temperatures) require a smaller amount of red muscle tissue to
support sustained swimming (Graham et al., 1983; Dickson, 1995).
B. White Muscle
The white muscle has a high anaerobic capacity fueled by glycogen (Guppy
et al., 1979; Hulbert et al., 1979; Arthur et al., 1992). Specific activities of LDH
are extraordinarily high in tuna, exceeding values from other scombrids (at the
same temperature-see Figure 8; Guppy and Hochachka, 1978; Dickson, 1995,
1996). This, in addition to large glycogen stores in the white muscle (145 pmol
g ml in skipjack, compared with 34 pm01 g -’ in rainbow trout; Arthur et al., 1992;

Schulte et al., 1992) indicates a high capacity for very fast, short-duration, swim-
ming bursts. This anaerobic swimming activity, and depletion of glycogen to pro-
duce ATP, can produce large amounts of muscle lactate (over 100 pm01 g - *, com-
pared with 42 pmol g-l in trout; Guppy et al., 1979; Arthur et al., 1992; Schulte
et al., 1992), and presumably a large metabolic acid load.
The resulting acidification from lactic acid production during burst swimming
activity is minimized by high blood and intracellular buffering capacities in tuna
(Perry et al., 1985; Dickson and Somero, 1987; Brill et al., 1992). The importance
of buffering in support of anaerobic glycolysis is indicated by the positive corre-
lation between buffering capacity and LDH activity in muscle of both marine
fishes and mammals (Castellini and Somero, 1981; Dickson, 1995). In an analysis
of five tuna and four ectothermic scombrid species, Dickson and Somero (1987)
found white muscle buffering capacity in tunas to be significantly higher (112
slykes compared with 99.5 slykes). By minimizing disruption of intra- and extra-
cellular pH that occurs during anaerobiosis, tunas may be able to increase the
duration, frequency, or velocities of burst swimming (Dickson, 1996).
In addition to a high anaerobic capacity, the white muscle of tunas also has
White Muscle
BLUEFIN TUNA (Thumwe
ALBACORE TUNA (Thunno

YELLOWFIN TUNA (Thunnus
SKIPJACK TUNA (Katsu%wwe
EL ACK SKIPJACK TUNA (Eufhynnue f&e
FRIGATE TUNA (Au& thazt#t@
STRIPED BONITO (Sarde orientef~~
E PACIFIC BONITO (Safda ch#iensk)

SIERRA MACKEREL (Scombervmorvus sierra)
PACIFIC MACKEREL (Scomberjeponicus)
0 500 1000 1500 2000 2500 3000 3500 4000
Lactate Dehydrogenase Specific Activity (U g -’ wet wt)
Fig. 8. Mean (?SE) lactate dehydrogenase (LDH) specific activity at 20°C in the white myoto-
mal muscle of tunas (solid bars) and ectothermic scombrid species (shaded bars). The white muscle
LDH activity in tunas is significantly greater than that for ectothermic scombrids. Data from Dickson
(1996 and unpublished observations ).
higher aerobic capacities compared with other fishes, including ectothermic scom-
brids (Guppy and Hochachka, 1978; Moyes et al., 1992; Dickson, 1996; Freund,
1999). The aerobic capacity is reflected in high Mb contents, and in some species
high capillarity (see above). As with the red muscle, mitochondrial volume den-
sity in skipjack white muscle (2-2.8%; Hulbert et al., 1979; Mathieu-Costello
et al., 1992; Moyes et aE., 1992) is within the range reported for other fishes (l-
4%; Johnston, 1981) and similar to that in Atlantic mackerel (Bone, 1978b). How-
ever, specific CS activities in white muscle of tunas are higher, even when com-
pared with ectothermic scombrids at the same temperature (Figure 9), suggesting
the intrinsic aerobic capacity of this tissue is elevated in the tunas (Hulbert et al.,
1979; Dickson, 1995,1996; Freund, 1999; Marcinek, 2000).
Although only the red muscle is supplied by well-developed countercurrent
heat exchangers, areas of the surrounding white muscle are also warmed via con-
duction from the deep red muscle. Recently caught fish or those exercised until
exhaustion show white muscle temperatures warmer than ambient water tempera-
ture (Carey, 1973; Graham, 1975; Graham and Dickson, 1981; Marcinek, 2000).
Archival tags placed beneath several centimeters of white muscle in large (ap-
White Muscle
BLUEFIN TUNA (Thunnus thyrmus)
ALBACORE TUNA (Thunnus ak&m@#

YELLOWFIN TUNA (Thunnus a/becxw@#
SKIPJACK TUNA (Ketwwnus~
BLACK SKIPJACK TUNA (Euthynnus linealvq
FRIGATE TUNA (Auxis thazardf
STRIPED BONITO (Sarda odentak)
E. PACIFIC BONITO (Sarda chitiensis)
SIERRA MACKEREL (Scomberomofuus s&m)

PACIFIC MACKEREL (Scomberjaponicus)
0 2 4 6 8 10 12 14 16
Citrate Synthase Specific Activity (U g -’ wet wt)
Fig. 9. Mean (*SE) citrate synthase (CS) specific activity at 20” C in the white myotomal muscle
of tunas (solid bars) and ectothermic scombrid species (shaded bars). Overall, white muscle CS ac-
tivity in tunas is significantly greater than that in ectothermic scombrids. Data from Dickson (1996
and unpublished observations).
proximately 100-250 kg) bluefin tuna report temperatures up to 10°C above am-
bient (Stevens et al., 2000; see Gunn and Block, this volume). The extent of
warming will vary with position relative to the body surface and the red muscle,
and the extent of red muscle excess temperature. As with the red muscle, an in-
crease in temperature can elevate the metabolic activity of the white muscle.
A clear difference between the endo- and ectothermic scombrids appears to be
that the capacity of white muscle to contribute to total aerobic capacity is actually
greater than the red muscle in tunas due to its high mass-specific aerobic capacity.
Although the aerobic capacity per unit gram of tuna white muscle tissue is less
than that of red muscle, because of its much larger mass, the potential contribution
of white muscle to total metabolic rate is greater. In tunas and other scombrids.
the white muscle accounts for approximately 45 to 55% of total body mass (Gra-
ham et al., 1983, Freund, 1999). In skipjack tuna, mass-specific CS activity is only
one-fifth that of red muscle (Moyes et al., 1992), but with about seven times as
much white muscle (Graham et al., 1983), total aerobic capacity in the white
muscle is about 40% greater than that of the red muscle. In yellowfin tuna, white
muscle as a whole has 8% higher aerobic capacity than the red muscle (Freund,
1999). In ectothermic scombrids the opposite is true; the red muscle has a greater
total aerobic capacity (11% in Pacific bonito and 64% in Pacific mackerel) than
the white muscle (Freund, 1999). This high aerobic capacity in tuna white muscle
likely supports rapid recoveries following anaerobic swimming bursts (discussed
further below). It also is possible that white muscle is recruited aerobically to
support high sustainable swimming speeds. In either case, it is clear that both the
aerobic and the anaerobic potentials of tuna white muscle are exceptional.
C. Other Tissues
Few studies have made an effort to quantify the activities of systems other
than those associated with locomotion or the circulatory system (Dickson, 1988;
Freund 1999). Freund (1999) measured aerobic activity levels (i.e., maximal CS
activity) and relative mass of the liver, kidney, gills, and caecum for yellowfin tuna
and Pacific bonito. From tissue mass and CS activities it was possible to calculate
the relative metabolic potential of these tissues (Table I). Freund (1999) found no
consistent difference in aerobic capacity, tissue mass, or relative metabolic poten-
tial between the two species. Taking relative mass into account, all of these tissues
together compose less than 10% of the total CS activity (Freund, 1999). The cae-
cum has the greatest contribution to total CS activity (2.1-3.6%) in both species
(Table I).
While CS activity indicates the potential for maximum aerobic activity, it is
not clear at what level these tissues regularly operate. The relative contribution of
each tissue to total metabolism will depend on the activity being performed and
its intensity.
Table I
Fractional Contribution (5 SE) of Four Tissues to
Total Citrate Synthase Activity (at 20°C) from
Yellowfin Tuna Thwvlus albacares (4.74 t 0.77 kg)
and Pacific Bonito Sat-da chiliemis (2.69 k 0.55 kg)
Fractional contribution of each tissue

(%I
Tissue Yellowfin Bonito
Liver 0.5 t- 0.06 0.3 t- 0.04

Kidney 0.53 2 0.07 0.45 ? 0.0
Pyloric caecum 2.13 2 0.25 3.57 ? 0.57
Gill 1.2 t 0.1 0.87 k 0.15
Total 4.36 5.19
Data from Freund ( 1999).
VI. MULTIPLE METABOLIC DEMANDS
Although much of the interest in tuna physiology has centered on swimming

adaptations, this is not the only metabolic cost that must be supported. Other, often
simultaneous, activities such as digestion and assimilation of prey, investment into
growth and reproduction, and repayment of the oxygen debt incurred during an-
aerobic swimming bursts also will contribute to aerobic metabolic demands.
Currently there are no measures of metabolic rate in tunas that can separate
out the costs of specific functions other than swimming and SMR. However, the
biochemical indexes of various tissues discussed above, as well as other evidence
(discussed below), indicate that metabolic processes other than aerobic swimming
are “high performance” in tuna with concomitant high energy costs (Brill, 1996;
Korsmeyer et al., 1996a). In tunas, as well as other fishes, these metabolic func-
tions may account for a large proportion of total metabolic rate, and can result in
conflicts if total demand exceeds aerobic metabolic scope (Priede, 1985).
We can divide the total respiratory or aerobic metabolism of a tuna into its
component parts (Priede, 1985; Korsmeyer et al., 1996a),
R = Rs + R, + R, + R, + RGBrR,
where R is the total aerobic metabolic rate, Rs is the &ndard metabolic rate, RF
is the metabolic rate attributable to the activities of digestion and assimilation,
also termed specific dynamic action (SDA), R, is metabolism due to aerobic loco-
motor activity, R, is due to recovery from oxygen debt, and RGsrRis growth and
reproduction.
2. TUNA METABOLISM AND ENERGETIC3 61
The metabolic costs of Rs (= SMR) and R, (aerobic swimming activity) are

discussed above. The following sections will discuss what is known about each of
the other metabolic components in tuna.
A. Specific Dynamic Action (RF)
A portion of ingested energy is lost due to the mechanical and biochemical

costs associated with digestion and assimilation, and this is defined as specific
dynamic action (SDA or R,; Jobling, 1981). R, in fishes accounts for about 15%
of ingested energy (Brett and Groves, 1979; Jobling, 1981). Maximum MO, fol-
lowing feeding in fishes generally ranges between 1.5 and 2.5 times SMR (Jo-
bling, 1981). In some fishes the MO, due to R, can equal the maximum active
MO, (Beamish, 1974; Priede, 1985).
Although no direct measurements have been made for tunas, R, is likely to be
a large component of aerobic metabolism because these fishes have high rates of
both consumption and digestion. Tunas can consume up to 30% of their body
mass per day (Kitchell et al., 1978), although the estimated daily ration for yel-
lowfin in the wild is between 4 and 7% of body mass (Olson and Boggs, 1986).
Based on postfeeding stomach contents, captive skipjack and yellowfin (24°C)
were found to empty their gut in an average of 12 and 10.4 h, respectively (Mag-
nuson, 1969; Olson and Boggs, 1986). This rate of gut clearance is 4 to 5 times
faster than for other piscivores of comparable size (Magnuson, 1969). In addition,
some species of tunas have the ability to elevate visceral temperature with vascular
retia (Collette, 1978; Stevens and Neill, 1978; Carey et al., 1984), presumably to
aid rapid digestion and assimilation. Stevens and McLeese (1984) found that the
elevated gut temperatures of bluefin tuna could increase the activity of digestive
peptidases by threefold. The ability to consume large amounts and rapidly clear
the gut enables tunas to take advantage of prey aggregations that are patchily
distributed, and still meet their high metabolic demands (Olson and Boggs,
1986). No examination of gut clearance or SDA has been made for ectothermic
scombrids.
B. Growth and Reproduction (R,;,,)
Tunas have relatively high rates of both somatic and gonadal growth (see
Sharp, this volume, and Schaefer, this volume). Growth rates vary considerably
between species and are linked to maximum size, which ranges from only a few
kilograms for Auxis sp. to over 680 kg for bluefin tuna (Collette and Nauen, 1983).
At an age of 1 year, yellowfin and skipjack tunas will have reached a mass of 2.3
and 1.3 kg, respectively (Wild, 1986; Uchiyama and Struhsaker, 1980). High
growth rates also are documented for other pelagic fishes. Dolphinfish and the
blue marlin will be 10 and 43 kg at 1 year, and reach maximum sizes of 46 and
580 kg, respectively (Palko et aZ., 1982; Uchiyama et al., 1986; Prince etal., 1990;
Nakamura, 1985).
In addition to growth, reproduction can be very costly. Skipjack produce about
100,000 eggs per kilogram per spawning (equal to approximately 2% of body
mass) and at times may spawn on a near daily basis over a 3-month period, pro-
ducing tens of millions of eggs annually (Forsbergh, 1980; Hunter et al., 1986).
For mature yellowfin tuna, the annual costs of spawning are estimated to be
equivalent to 254% of body mass in females and 120% in males (Schaefer, this
volume). These annual reproductive costs as a proportion of total energy expen-
diture are estimated to be 17.5 and 8.8% in females and males, respectively. Al-
though the metabolic costs for growth and reproduction in tunas are high, other
large, tropical, pelagic fishes may have similar costs.
C. Oxygen Debt Recovery (R,)
Anaerobic metabolism can elevate energy expenditure beyond the aerobic

scope, but ultimately will result in the aerobic costs associated with R,. Short
periods of high-intensity swimming, powered by anaerobic metabolism of the
white muscle, result in depletion of glycogen reserves, buildup of lactate, depres-
sion of blood pH, and ionic and osmotic disturbances (Wood, 1991). These phys-
iological disturbances may result in exhaustion and inability to perform further
burst swimming activity. Recovery from exhaustive exercise is associated with an
elevation in MO,, “repaying” the oxygen debt, while restorative processes take
place.
Recovery from anaerobic activity involves removal of lactate and return of
acid-base balance, processes which require energy provided by oxidative (aero-
bic) metabolism (Moyes et al., 1993). Despite generation of high, postexercise
lactate levels, these processes occur very rapidly in skipjack tuna (<90 mitt; Perry
et aE., 1985; Arthur et al., 1992), many times faster than in rainbow trout (6-24
h; Milligan, 1996). The majority of lactate is resynthesized to glycogen within the
white muscle (Weber et al., 1986; Arthur et al., 1992; Buck et al., 1992). Rates of
lactate clearance from white muscle in skipjack (1.3 pmol g-l min-I; Arthur
et al., 1992) are lo- to lOO-fold greater than those in other fishes (0.011-0.125
prnol g-l min-I; reviewed by Moyes et al., 1993), and there is a close correlation
with the repletion of muscle glycogen and phosphocreatine (Arthur et al., 1992).
These rates were measured in fish prevented from swimming, which may have
impeded recovery. Milligan et al. (2000) recently found that rainbow trout allowed
to swim at low speeds recovered much faster (<2 h) than those held in still water
(>6 h). The rapid recovery in tuna permit burst swimming to occur with greater
frequency.
White muscle aerobic capacity strongly correlates with the rate of lactate
2. TUNA METABOLISM AND ENERCiETICS 63
clearance in fishes (Moyes et al., 1993). This suggests that the high aerobic capac-
ity of tuna white muscle may function for rapid recovery from the large lactate
load generated in the white muscle during burst swimming (Dickson, 1995; Kors-
meyer et al., 1996a). It also suggests that oxygen debt recovery in tunas can be a
major component of total oxygen demand (Bushnell and Brill, 199 I ; Brill, 1996;
Korsmeyer et al., 1996a).
D. Modeling Multiple Metabolic Costs
Based on measured rates of growth, caloric intake and digestion, lactate clear-
ance and creatine rephosphorylation, and swimming metabolism, Korsmeyer et al.
(1996a,b) calculated estimates of the average potential aerobic costs associated
with each metabolic component (Figure 1O).3 This model of tuna metabolic de-
mands is based on a 2-kg yellowfin tuna, because the best estimate of swimming
metabolic rates and most other physiological data are from tunas of this size and
at a temperature of about 25°C. Actual measurements of the metabolic costs as-
sociated with these processes in tunas and other pelagic fishes would be a useful
area for future research. However, this model analysis provides us with an estimate
of how various metabolic functions of tunas contribute to total energetic demands,
and how they may fit within the aerobic scope.
It is clear that tunas have elevated energy demands for many metabolic pro-
cessesin addition to aerobic swimming and SMR (Figure 10). This is particularly
true for oxygen debt recovery. The estimated h;IO, required for oxygen debt re-
covery (840 mg 0, kg--’ h-0 approaches that of high-velocity aerobic swimming
(1100 mg 0, kg-’ h-l above SMR at 3.5 L s-l). This is not surprising given that
the total aerobic potential of white muscle, the site of glycogen resynthesis, ex-
ceeds that of red muscle in tunas (see above).
All fishes have a potential power budgeting problem in that the combined
capacities for R,, R,, and R,, in addition to Rs, will likely exceed maximum
aerobic capacity (Priede, 1985). Conflicts in oxygen demand between digestion
and swimming activity, for example, have been demonstrated in a number of
fishes. In the sablefish Anaplopoma fimbria, as swimming oxygen demand in-
creases, the proportion allocated to digestion decreases until swimming consumes
all of the metabolic scope (Furnell, 1987). Alternatively, in rainbow trout the costs
‘These values must be taken only as a first approximation as none of the estimated values will be
constant. MO,, due to R, increases to a maximum following feeding and then declines over many
hours, and its magnitude will depend on the quantity and quality of prey (Jobling, 1981). Growth rates
are higher in younger tuna and decrease with age (Wild, 1986), and part of this cost may be included
in SMR or R, (Jobling, 1981). Oxygen debt recovery is maximal just after intense exercise and de-
clines with time, and additional costs are associated with readjustment of ion, acid-base, and fluid
volume disturbances (Wood, 1991). Therefore, these values may actually underestimate costs in many
cases.
3000
- growth
2500
2000
1500 --
- 3.5 L s-
1000
500 --
- 1 L s-l
0
Fig. 10. Potential aerobic energetic costs estimated for a 2.1-kg (50 cm) yellowfin tuna (Thunnus
albacares) at 25°C. Included are standard metabolic rate (SMR), aerobic swimming costs, oxygen
debt recovery, specific dynamic action (SDA), and growth (Korsmeyer ef al., 19!96a,b). Swimming
costs are given at both 1 .O body length (L) per second and at 3.5 L s-l, which is predicted to be near
the maximal sustained swimming speed (Korsmeyer er al., 1996b; Brill, 1996). Total aerobic costs, if
all processes occur simultaneously (273 1 mg O* kg -’ h-l), are near estimates for maximal metabolic
rate in tuna (2500 mg O2 kg-’ h-l). This suggests that the tuna’s aerobic scope can support multiple
metabolic processes without conflicts in oxygen delivery.
of R, are not reduced, but instead limit swimming velocities once maximal MO,
is reached (Alsop and Wood, 1997).
These conflicts occur due to limitations of the cardiorespiratory system to de-
liver sufficient oxygen to competing tissues. During exercise in fishes, blood flow
to the viscera is reduced and redistributed to the red muscle (Randall and Dax-
boeck, 1982; Axelsson et al., 1989; Axelsson and Fritsche, 1991; Thorarensen
et al., 1993). This redistribution likely reflects the inability of the circulatory sys-
tem to supply sufficient oxygen to viscera (for digestion) while also supporting
the aerobic locomotory muscles. In fish with higher oxygen delivery capacities
(higher hematocrit), there is less reduction in visceral blood flow (Thorarensen
et al., 1993). Clearly, aerobic scope determines the extent to which multiple func-
tions can occur simultaneously.
In tunas this problem is made especially acute by a high R, and the constant
swimming requirements (R,) required for gill ventilation and hydrodynamic lift
(Magnuson, 1973). After feeding, tunas must be able to repay any oxygen debt
incurred during prey capture and rapidly complete the processes of digestion to
prepare the gut for the next prey encounter. All of these various metabolic oxygen
requirements can and do occur simultaneously, heightening potential conflicts in
oxygen demand.
Total aerobic metabolic costs, however, cannot exceed the MMR. If, however,
as data from skipjack suggest, MMRs for tuna are 2500 mg 0, kg-’ h-l (see
above), then significant aerobic scope (2200 mg 0, kg-’ h-~‘) would be available
to support multiple metabolic functions, even beyond that required for high sus-
tained swimming speeds. For example, a tuna could support its SMR, deliver suf-
ficient oxygen to the red muscle for swimming continuously at moderate veloci-
ties, and still have sufficient aerobic scope to support rapid lactate clearance in the
white muscle tissue (Figure 10; Bushnell and Brill, 1991). In this way, tunas do
not need to rest (something they cannot do) following exhaustive exercise, but can
continue to search for prey to support their high energy demands while clearing
the gut and replenishing white muscle glycogen stores in preparation for the next
bout of burst swimming. In fact, the highest measured &IO, in tuna was from
skipjack that were just caught from a feeding frenzy and were therefore likely
repaying an oxygen debt and digesting prey, while also swimming at 3.5 L s ’
(Gooding et al., 198 1). The large aerobic metabolic scope of tunas may, therefore,
be an adaptation to limit conflicts among the simultaneous requirements of mul-
tiple metabolic demands (Priede, 1985; Brill, 1996: Korsmeyer et al., 1996a).
VII. DISCUSSION AND CONCLUSIONS
Above we have summarized the available information examining the meta-

bolic costs in tuna, the associated adaptations, and the estimated relative contri-
butions of different components. Tuna energetics has a long history and much has
been learned in the last 20 years. The recent addition of data from ectothermic
scombrids and other active teleosts provides greater power for examining the sig-
nificance of different traits and compels us to reexamine conclusions based only
on comparisons with salmonids. Much remains to be done, but for now let us
revisit the questions posed in the Introduction.
A. How Does the Metabolic Rate of Tunas Compare

with Other Fishes?
Regardless of the method used it is clear that tunas have high energetic costs.
The primary basis for this is the elevated SMR, which is also reflected in an ele-
vated swimming metabolic rate. While the SMR in tuna is higher than that found
in many species, comparable values are found in other large, active (but ecto-
thermic) species such as the dolphinfish and bonito. In general, fishes with a
greater aerobic scope for activity also have a high SMR (Priede, 1985). This rela-
tionship suggests that a high SMR is related to the costs of supporting the phys-
iological systems required for a high MMR, and would agree with MMR estimates
for tunas. Consequently, an elevated metabolic rate does not depend on endoth-
ermy, but may be associated with capabilities for enhanced activity and an in-
creased metabolic scope (i.e., permits higher MMRs).
What accounts for the high SMR of tunas and some other pelagic fishes? One
hypothesis is that the large surface area and tbin epithelia of the gills entails a high
osmoregulatory cost and consequently an elevated SMR (Brill, 1987, 1996). For
some fish there appears to be a general positive correlation between SMR and gill
surface area (Brill, 1996). For others this does not hold true. Both the mackerel
and the menhaden (Brevoortia ryrunnus) have mass-specific gill surface areas that
exceed either the bonito or the dolphinfish (Gray, 1954), yet they have lower meta-
bolic rates (Figure 1; Sepulveda and Dickson, 2ooO; Freund, 1999). Elevated os-
moregulatory costs in tunas are suggested by high estimates for gill MO, in spi-
nally blocked skipjack and yellowfin tunas (50-70% of MO,; Bushnell and Brill,
1992) compared with other fishes (27% of MO, in rainbow trout; Daxboeck et al.,
1982). However, estimates based on tuna gill Na+-K+ ATPase activity are much
lower (9-13% of SMR; Brill and Bushnell, this volume). Other factors which
could cause elevation of SMR include an increase in the proton leak across the
inner mitochondrial membranes (Brand, 1990) costs of maintaining metabolic
machinery (e.g., enzyme turnover), and high rates of growth.
Although the SMR and RMR of tunas may be comparable to some other active
fishes, we predict that MMR will be greater. The total aerobic metabolic potential
in tunas is increased, even in comparison with ectothermic scombrids, by red
muscle endothermy and an extraordinary white muscle aerobic capacity.
B. What Are the Adaptations Related to Supporting

the Energetic Demands of Swimming
and Other Metabolic Processes?
Each step in the oxygen cascade from the gill to the mitochondria is special-
ized to enhance oxygen &IX in tuna. The structure of the gills facilitates increased
levels of oxygen uptake from the water. A large heart generates high rates of blood
flow, and oxygen uptake at the tissue is improved by the capillary structure and
tissue Mb concentrations. In the tissue, the ability to produce ATP is enhanced by
elevated activities of metabolic enzymes, Compared to other scombrids, tuna red
muscle aerobic capacity is elevated not by great increases in specific enzyme
activities, but by a greater amount of tissue in some species, and the ability to
2. TUNA METABOLISM AND ENERGETIC3 67
increase the temperature of this tissue. The white muscle of tunas has higher in-
trinsic anaerobic and aerobic capacities than other fishes, including scombrids.
Interestingly, these same patterns have been observed in white muscle of endo-
thermic and ectothermic sharks (Dickson et al., 1993).
C. How Do Tuna Energetics Relate

to Their Swimming Performance?
Perhaps the most surprising finding is that, based on the available data, tuna
are no more efficient swimmers than other active fish, including mackerel and
salmon. This seems unlikely given the suite of apparent hydrodynamic and bio-
mechanic specializations in tunas. There are a number of possible reasons why
this is the case: (1) It may be that any energetic advantages are slight, and that our
current data are constrained by the technical challenge of working with these
fishes and limited comparative data on large, active fish at the same temperature.
(2) The energetic advantages may not be apparent during the steady swimming
recorded in a swim flume or metabolic chamber, but instead are manifestedduring
a swim-and-glide mode of swimming which is hypothesized to increase efficiency
(Weihs, 1973). The extensive streamlining may act to minimized drag during pe-
riods of gliding, rather than when the body is undulating. Observations of free-
swimming captive fish and during acoustic telemetry in the field indicate that tu-
nas use this mode of travel (Holland et al., 1990; Block et al., 1998; H. Dewar,
personal observation). (3) Alternatively, tuna morphology may be an adaptation
for rapid accelerations, aiding anaerobically powered, high-speed burst swim-
ming and prey capture. (4) Finally, tuna specializations may allow higher sustain-
able (aerobic) swimming speeds, without improving efficiency. For example, ele-
vated red muscle temperatures could increase power output, without necessarily
reducing the cost per unit power produced. This will increase the speed at which
the transition to white muscle recruitment must occur. For this last possibility,
some limited data are available.
Maximal sustained4 swimming speed (U,,,,) has not been directly measured for
~Swimming activity is usually classified into several categories which define the duration over
which the fish can perform at that level of activity, as well as the metabolic pathways which provide
the energy for the different types of swimming. Sustained swimming is that which can be maintained
indefinitely (for practical purposes, considered 200 min or longer) without resulting in fatigue and
which is supported by aerobic metabolism. Prolonged swimming is that which results in fatigue be-
tween 20 s and 200 min. Prolonged speeds are supported by aerobic metabolism as well as some
anaerobic component. The critical swimming speed (U,,,) is a subcategory of prolonged swimming
and is determined experimentally by enforcing stepwise increments in swimming velocity until fatigue
occurs. The U,,,, is then calculated as the highest velocity the fish could maintain for a defined period
of time (usually 30 to 60 mm). Burst swimming speeds are the highest speeds of which the fish is
capable, result in rapid fatigue ( c2f) 6). and are predominately supported by anaerobic metabolism
(Jobling. 1994).
tunas, although claims of extraordinary values (6-10 L s-l) have been reported
(Yuen, 1970; Beamish, 1978; Dizon et aE., 1978; Magnuson, 1978). However, the
highest swimming velocities of tunas (30-200 cm in length) tracked in the wild
or held in captivity are generally less than 3 L s-l (reviewed in Bushnell, 1988,
and Korsmeyer et al., 1996a; Block et al., 1998; Brill et al., 1999). The highest
velocities achieved in a water tunnel for skipjack and yellowfin tuna (30-51 cm)
were 3 L s-l or less, for periods of 40 to 60 min (Dewar and Graham, 1994).
Models of oxygen uptake, swimming energetics, and tissue oxygen delivery sug-
gest that tunas have a II,,,, between 2 and 4 L s-’ (for -50-cm tuna; Brill, 1996;
Korsmeyer et al., 1996b). These data suggest that II,,,, values in tunas are much
less than early reports suggested.
Comparison of these estimates with II,,,, in other fishes is complicated by lack
of data for similarly sized fish at the same temperature. However, the above values
for tuna overlap measured U, values for other fishes. In a summary of 25 fish
species, ranging from 5 to 55 cm, Videler (1993) found an average U, of 3.3 L
s-l, varying from 1.4 to 4.8 L s-l. Among fish of larger size (-55 cm), U,, was
as high as 3.1 and 3.3 L s-l in sockeye salmon (lS”C), and pink salmon (Oncor-
hynchus gorbuscha, 2O”C), respectively (Brett, 1982). Therefore, U, in tunas ap-
pears to be similar to or only slightly higher than that in other fishes. Further
indicating that swimming performance in tunas is not exceptional, critical swim-
ming velocities4 (maintained for 30 min) among small (18-22 cm) kawakawa and
yellowfin tuna (I-I,, = 3.2-4.7 L s-l) are not significantly different from another
scombrid, the Pacific mackerel (3.8-5.8 L s-l; Sepulveda and Dickson, 2000).
Tunas do have higher optimal swimming velocities, suggesting they are
adapted for higher routine swimming speeds, but this is accompanied by higher
swimming costs (Figure 5). Clearly, to resolve the question of swimming effi-
ciency, additional research is required. Potential lines of research include: (1)
studies with free-swimming tuna using an indicator of energetic output (e.g., tail
beat or heart rates), (2) experiments with larger fish, given the changes in mor-
phology (Magnuson, 1978) and potential increases in excess muscle temperatures
with body size, and (3) advancement of biomechanical models that allow indirect
estimates of thrust and drag based on kinematics.
D. What Metabolic Processes Account for the Total

Energetic Costs in Tunas?
Although we cannot produce an energy budget for tunas because we do not

know how much time is spent in any particular activity, the information reviewed
above provides us with an estimate of the potential metabolic costs. SMRs in
combination with aerobic swimming costs are high. U,, for a 2-kg (-50 cm)
yellowfin tuna is similar to routine speeds measured in the field (2 L s-l, Holland
et al., 1990). At this velocity, two-thirds of the total costs (-700 mg OZkg-’ h- I)
are associated with locomotion and one-third with SMR (Dewar and Graham,
1994). Although MMR is not well defined, it appears that even at this speed a
considerable fraction of aerobic scope remains.
As maximal sustained swimming speeds in tunas do not appear to be extraor-
dinary, their high aerobic scope could be an adaptation that permits the provision
for other metabolic costs on top of a high SMR and continuous locomotion. The
potential contributions of reproduction, growth, digestion, and recovery from an-
aerobiosis are likely also high in tunas. A high aerobic scope would limit potential
conflicts in energy demand, including that required for growth and reproduction
(= Darwinian fitness). Among these other metabolic costs, recovery from intense
anaerobic activity has the highest potential for oxygen demand.
Tuna white muscle differs from that of other fish, including other scombrids,
in that in conjunction with a high anaerobic capacity, this tissue has an extraordi-
nary aerobic capacity. Total aerobic capacity of the white muscle in tunas exceeds
that of the red. This aerobic capacity is likely associated with the tuna’s capabili-
ties for rapid oxygen debt recovery. Rapid recovery, while also swimming at mod-
erate aerobic velocities, will permit more frequent swimming bursts (- 10 L s. ‘;
Magnuson, 1978), and can therefore result in higher average swimming veloci-
ties. Videler and Weihs (1982) have proposed that use of the white muscle in a
burst-and-coast mode of swimming would be more efficient than swimming con-
tinuously at high velocities. This may account for the extraordinarily high speeds
reported for some schools of tuna (Yuen. 1970).
E. Finally, How Does the Metabolism of Tunas Relate to

Their Pelagic Existence and the Evolution of Regional
Endothermy?
This question is best separated into two sections. First we examine the tuna’s
adaptations in relation to their pelagic existence. Tunas are often called energy
speculators (Stevens and Neill, 1978), investing large amounts of energy (high
SMR) on the potential for high energy returns in prey capture. Although it may
appear that a high SMR is a disadvantage, this supports the capacity for increased
levels of oxygen uptake, delivery, and utilization, and consequently work. The
resulting high MMR and aerobic scope not only enable tuna to carry out many
metabolic functions at a faster rate than other fish, but to do so simultaneously,
reducing energetic compromises. Rates of work are, of course, enhanced by ele-
vated temperature as well. Rather than minimize energy expenditure, tunas maxi-
mize energy intake, increasing the ratio of energy income to energy output. In
many respects the metabolic intensity of tunas parallels that of other endotherms
(mammals and birds); the increase in aerobic scope allows access to greater en-
ergy resources and ultimately increased fitness. The recent similarities observed
between tuna and some other active pelagic fishes have not changed this conclu-
sion-it is just clear that tuna are not the only energy speculators.
The evolution of endothermy has been the subject of great interest for scien-
tists focusing on both marine and terrestrial vertebrates, Energetics has been the
focal point of many studies of endothermy due to the 5- to lo-fold difference in
resting metabolic rate between endo- and ectothermic terrestrial vertebrates (Else
and Hulbert, 1981, 1985). In tunas it does not appear that a regional elevation in
body temperature necessarily results in an elevated metabolic rate when compari-
sons are made at the same activity level. The SMR or RMR is similar for tunas,
bonito, and the dolphinfish (Figures 1 and 3A). Instead, it is the maintenance of
suite of adaptations (SMR) that facilitate a high aerobic scope and account for that
elevation (see above). What increases as a result of elevated temperatures is the
maximum rate and which functions can be performed, as indicated by thermal
affects on muscle performance (Altringham and Block, 1997; see Altringham and
Shadwick, this volume) and digestion (Stevens and McLeese, 1984). Thus, while
not apparent in the SMR and RMR, when the metabolic costs are measured over
a broader range of activities, an elevation in tuna &IO, may be apparent.
In addition to examining the potential cost of endothermy, the tunas and their
ectothermic sister taxa provide an ideal opportunity to examine the evolution of
endothermy (Dickson, 1995, 1996; Freund, 1999). Important questions center
around the advantages of endothermy and the necessary physiological precursors.
There are two dominant theories as to why endothermy evolved: (1) to expand the
thermal niche, and (2) as a byproduct of selection for increased aerobic capacity.
We are currently not in a position to resolve this question (but see Block and
Finnerty, 1994; Brill et al., 1999), and these two possibilities are not necessarily
mutually exclusive. Further information on phylogenetic relationships, metabolic
capacity, and thermal range is needed. The high RMRs of bonito, but not mackerel
(Freund, 1999), suggest that an increased aerobic capacity evolved prior to the
evolution of endothermy within the scombrids. Certainly, one advantage of en-
dothermy is a further increase in the aerobic capacity of the red muscle (Dickson,
1996) and possibly the white muscle, but the consequences on tuna swimming
ability remain elusive.
VIII. THE FUTURE
Although our understanding of tuna energetics has been improved, much re-
mains to be done. Actual measurements of many metabolic costs (SDA, oxygen
debt recovery, maximal metabolic rates) are needed to fully understand the con-
sequences of a high SMR and tissue aerobic capacities. Our interpretation also has
been restricted by the limited scope of species studied. Most research has been
conducted on juveniles of a few tropical species and clearly not all tunas are
created equal. Within the tuna clade exists a great deal of morphological and phys-
iological variation. Our conclusions may change when additional data are ob-
tained on other tunas that inhabit cooler waters, such as the albacore, bigeye, and
bluefin tunas. These species have greater endothermic capabilities, with greater
temperature elevation and more regions served by countercurrent heat exchangers
(Carey, 1973; Stevens and Neill, 1978). Comparisons within the thunnini tribe.
and over a greater range of size, would be useful for examining the functional
significance of endothermy and both scaling and ontogenetic effects. Studies of
other pelagic fishes, and the endothermic sharks, will also be of great use in teas-
ing out the selective pressures of an oceanic environment and the evolution of
endothermy.
ACKNOWLEDGMENTS
For their helpful comments and critique on drafts of the manuscript, we gratefully thank Rich
Brill, Kathy Dickson, Don Stevens, Barb Block, and Tony Farrell. Also, we thank Kathy Dickson,
Chugey Sepulveda, Ellen Freund, Dave Marcinek, John Steffensen, and Robert Shadwick for access
to unpublished data. Any errors in this chapter, however, are solely those of the authors. Support for
the preparation of this manuscript was provided to H.D. by the Pfleger Institute of Environmental
Research and to K.E.K. by Hawaii Pacific University Trustees’ Scholarly Endeavors Program.
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3
THE CARDIOVASCULAR SYSTEM OF TUNAS

RICHARD W BRILL
PETER G. BUSHNELL
I. Introduction
II. Cardiovascular Function at Routine Activity Levels
A. Oxygen Transport from Water to Tissues
B. High Blood Pressures and the Maintenance of Tissue Fluid Balance
III. Maximal Rates of Cardiovascular Function in Tunas
A. How Skipjack and Yellowfin Tunas Achieve High Maximum Metabolic Rates
B. Elevated Hematocrit, Oxygen Transport, and Blood Viscosity
IV. Tuna Cardiac Function
A. Stroke Volume
B. Maximal Heart Rates in Tunas and Other Teleosts
C. Sarcoplasmic Reticulum
D. Mechanical and Electrical Coupling of Myocytes
E. Biochemical Adaptations of Tuna Hearts for High Power Output
F. Ventricular and Arterial Dynamics and Functions of the Bulbus Arteriosus
V. Cardiac Function and the Physiological Ecology of Tunas-A Possible Connection
VI. Summary and Conclusions
I. INTRODUCTION
Tunas (family Scombridue, tribe Thunnini) have high metabolic rates (Kors-
meyer and Dewar, this volume) and are obligate ram ventilators (Brown and Muir,
1970; Roberts, 1975, 1978). They suffocate rapidly if prevented from swimming
so special care must be taken to ensure that ventilatory requirements are met dur-
ing all stages of an experiment. Tunas also struggle violently during any restrain-
ing procedure. It is impossible to use completely intact, unanesthetized, “resting”
fish to make even the simplest cardiorespiratory measurements using techniques
commonly employed with other species (e.g., Smith and Davie, 1984; Smatresk,
1986). Some data have been obtained on swimming tunas (Jones et al., 1990,
1993; Bushnell and Brill 1991; Korsmeyer et al., 1997a,b) but these procedures
are inherently very difficult and fish can carry only minimal instrumentation with-
79
80 RICHARD W. BRILL AND PETER G. BUSHNELL
out impacting hydrodynamics and increasing metabolic energy demand (Kiceniuk

and Jones, 1977; Jones et al., 1990). Much of the data on tuna cardiovascular
function has, therefore, been recorded in somewhat unusual circumstances such
as total neuromuscular blockade with forced ventilation (Stevens, 1972; White
et al., 1988) or spinal blockade with fish in a water stream (Bushnell and Brill,
1992). Tunas are also expensive to acquire, difficult to maintain in captivity, and
are routinely kept in shore side tanks at only a handful of laboratories (Nakamura,
1972; Brill, 1999; Farwell, this volume). The difficulties of working with indi-
vidual fish are compounded because relatively few animals are available for study.
As a result, our understanding of cardiovascular function in tunas is incom-
plete. This should not be construed to mean that it remains a mystery. On the
contrary, in spite of the difficulties of working with these fishes, there exists a
significant body of publications that range from the molecular and biochemical to
whole-animal physiology. In this chapter we synthesize the more recent of these
diverse studies and endeavor to show how they are beginning to present a unified
picture of these fascinating animals.
We start our discussion by attempting to distinguish which aspects of the car-
diovascular system of tunas are clearly enhanced compared to other teleosts. For
the following reasons, however, we do so with only a modest degree of certainty.
Rates of virtually all physiological functions are influenced by temperature and
scale nonlinearly with body mass. Yet correcting for these variables, and mak-
ing appropriate comparisons, can be problematic because temperature effects and
scaling relationships are often ill-defined (Packard and Boardman, 1999). This is
especially true when comparing rates of cardiovascular function in tunas to those
of other teleosts. Because of their accessibility, most of our knowledge of teleost
cardiovascular physiology comes from measurements made on temperate (i.e., at
<2O”C), small (cl kg body mass), freshwater fishes (e.g., rainbow trout, Onco-
rhynchus mykiss). In contrast, information on tuna cardiovascular function comes
mostly from measurements made on l- to 3-kg skipjack tuna (Katsuwonus pe-
Zumis) and yellowfin tuna (Thunnus al&cures) at 25” C. Data at = 15” C are avail-
able for albacore (Zhnnus ululungu), but are from fish of ~7-10 kg body mass
(Lai er al., 1987; White et aZ., 1988; Graham et al., 1989). Also, albacore are not
routinely maintained in captivity and all in vivo data have been collected at sea on
recently captured fish when they may have been physiologically stressed and re-
covering from exhaustive exercise. The different methods used to quantify cardio-
vascular function in tunas and other teleosts can also generate what appear to be
species-specific differences, but that are artifactual (Metcalf and Butler, 1982;
Kalinin et uE., 1999). Therefore, as in all experiments involving whole animals,
but more so with tunas, the anesthesia, surgical, handling, and instrumentation
procedures required to make cardiovascular measurements can easily distort the
very processes being evaluated.
We also attempt to discern the important functional adaptations that set tunas
3. THE CARDIOVASCULAR SYSTEM OF TIJNAS Xl
apart from other teleosts. In theory, this type of analysis should involve compari-
sons of more than two or three species, include data from “primitive” tnembers
of the clade, and employ statistical procedures that take phylogenetic distances
into account (Garland and Adolph, 1994). In our case, the application of these
principles is problematic as the in uivo data on tuna cardiovascular physiology
come from only three species: skipjack tuna, yellowfin tuna, and albacore. More-
over, although critical for discerning the evolution of cardiovascular function, the
physiology of primitive members of the family Scumbridue (the so-called “ecto-
thermic scombrids”) remains almost unstudied. [The ectothermic scombrids in-
clude the bonitos (tribe Surdini). seerfishes (tribe Scomberomorini), and mackerel
(tribe Scombrini).]
II. CARDIOVASCULAR FUNCTION AT ROUTINE

ACTIVITY LEVELS
Besides being obligate ram ventilators, tunas also depend on constant forward
motion to produce lift from their pectoral fins for hydrostatic equilibrium (Mag-
nuson, 1978; Magnuson and Weininger, 1978). If tunas stop swimming they sink
as well as suffocate. As a result, throughout this review we refer to “routine” rates
of cardiovascular function. By this we mean those associated with swimming
speeds ranging from 1 to 2 body lengths s ‘, This level of activity is commonly
recorded when skipjack and yellowfin tunas are able to set their swimming speeds
either in the laboratory, or when fish carrying ultrasonic transmitters are followed
in the open ocean (e.g., Dizon et al., 1978; Dizon and Brill, 1979; Gooding et al.,
1981; Holland et al., 1990b; Block et al., 1997; Brill et al., 1999; Freund, 1999).
Table I summarizes the anatomical and physiological descriptors of cardio-
vascular function in tunas that we regard as the most reflective of unstressed ani-
mals. We have highlighted in bold those values we consider unusual in tunas, and
on which we will focus. For comparison, we have included data from yellowtail
(Seriola spp.) and rainbow trout. We selected the former because they are active,
pelagic, warm-water, marine fishes, and because data are available from a range
of body masses similar to those of skipjack and yellowfin tunas commonly used
in physiological experiments. We chose the latter because it is the most well-
studied teleost species in terms of its physiology, and because data are available
on minimal as well as maximal rates of cardiovascular function.
The standard metabolic rates (i.e., those measured in fish paralyzed with neu-
romuscular blocking agents) of skipjack and yellowfin tuna are 412 and 286 mg
0, kg ’ h-l, respectively (Brill, 1987), values several times those of yellowtail at
“rest.” At routine swimming speeds (= 1-2 body lengths s- ‘), the metabolic rates
of skipjack and yellowfin tunas are 974 and 776 mg 0, kg ’ h-‘, which are
approximately six to eight times that of yellowtail, a marine species living at a
Table I
Cardiorespiratory Function in Tunas and Other Teleosts
Yellowfin Skipjack
tuna” tunaa Yellowtail b Rainbow trout’
Temperature 25°C 25OC 19-25°C 10°C 10°C

Body mass (kg) -1-2 =l-2 =1 0.9-1.5 0.9-1.5
Swimming speed (body lengths SE’) 1.0-1.3 1.6-2.2 =0.5-1.58
Activity level Routine h Routine Rest Rest Maximum
sustainable
Total O2 consumption (mg 0, kg ’ h-‘) 776 974 138 48 312
Gill O2 consumption (mg 0, kg-~’ h-‘) 362 420 2 -0 213
Body O2 consumption (mg 0, kg-’ h-l) 414 554 136 54 159
Ventilation volume (liter min-’ kg-‘) 2.4-4.7 3.8 0.46 0.5 1.7
Utilization (%) 51-59 52 25 33 33
TO, (mg 0, mini’ kPa-’ kg- ‘)” 0.030 0.056 0.00076 0.0038
Ew WV’ 63 67 42 37
6 (WY 89 74 73 100 -
PaO, (kPa)’ 10-12 9.3 10.6 18.3 16.8
P,O, &Pa)’ 5.2-5.3 4.9 4.4 2.1
C,O, (mg dlm’)e 18 20 16 15 14
C,O, (mg dl-I)* 12 13 9.5 10 1.9
0, delivery (mg 0, min-’ kg-l)’ 21 26 5.6 2.1 7.4
Ventilation perfusion capacity-rate ratiod 0.73 1.1 0.55 1.2-2.0 2.2
Hematocrit (%)< 27-35 34-38 29 23 27
Hemoglobin concentration (g dl-‘)e 11-12 13 11 6.4 -
Mean cell hemoglobin concentration (g dl- 31-44 34-38 38 29 -
Gill surface area (cm2/kg body mass) 14380 18,400 ==2ooo
Gill blood-water barrier thickness (pm) 0.533 0.596 6.37
Blood volume (ml kg-‘) 3 l-54 =50 58 41-52 -
Cardiac output (ml min 115 132 35 18 53
62-97 19 96 38 51
Stroke volume (ml kg-‘)’ 1.1 1.3 0.35 0.46 1.03
Mean VA blood pressure (kPa)’ 10.8-11.8 11.6 5.8 5.2 8.3
Mean DA blood pressure (kPa)= 6.7-6.8 5.3 1.4 4.1-4.5 -
Gill resistance (kPa ml-l min-’ kg-‘)’ 0.035-0.044 0.047 0.12 0.039-0.061 -
Systemic resistance @Pa ml-’ min.’ kg-‘)c 0.058-0.059 0.040 0.040 0.23-0.25 -
Total resistance (kPa ml-’ min ’ kg ‘) * 0.094-0.10 0.088 0.17 0.29 0.16
Ventricle mass (% body mass) 0.29 0.38 0.11 0.08-0.13 0.08-0.13
Cardiac power output (mW kg-’ body mass)’ 21-23 26 3.4 1.6 7.1
Cardiac power output (mW g.-’ ventricle mass) 7.1-7.8 6.7 3.1 1.2-1.9 5.6-9.1
Nom: Those parameters that we consider clearly enhanced in skipjack and yellowfin tunas are printed in bold.
‘Data for yellowfin (Tizunnus dbucures) and skipjack (Kutsuwonus pelamis) tunas compiled from Muir and Hughes
( 1969); Bushnell (1988); Bushnell et al. (1990); Jones et al. (1986, 1990, 1993); Brill and Bushnell (1991); Bushnell and
Brill(l991, 1992); Dewar (1993); Brill and Jones (1994); Dewar and Graham (1994); Korsmeyer et al. (1997a.b); Brill
r~ al. (1998): Lowe et al. (1998); and R. Brill, T. Lowe, and K. Cousins (unpublished data).
@Data for yellowtail (Seriola spp.) compiled from Yamamoto et al. (1981); Itazawa er al. (1983); and lshimatsu et
ul. ( 1990, 1997).
-Data for rainbow trout (0rrcorfrynchu.s mykiss) compiled from Holeton and Randall (1967); Randall et al. (1967);
Stevens and Randall (1967); Kiceniuk and Jones (1977); Gngerich et al. (1987, 1990); Tetens and Christensen (1987);
Palzenberger and Pohola (1992); and Farrell and Jones (1992).
“Data for skipjack and yellowfin tunas from spinally blocked (i.e. nonswimming) fish
‘Data for skipjack tuna from spinally blocked (i.e., nonswimming) fish.
‘Cardiac power output is calculated as cardiac output multiplied by mean ventral aortic (VA) pressure.
8As a result of the extra hydrodynamic drag induced by the catheters and wires required to measure heart rate, blood
pressures, etc., maximum sustainable swimming speeds were below those of uninstrumented fish (-2 body lengths ss’).
similar temperature (Table I). Clearly, the cardiovascular and respiratory systems
of skipjack and yellowfin tunas must supply oxygen and metabolic substrates to
the tissues at exceptional rates, and hence we often use the term “high-energy-
demand fishes” as a general descriptor (e.g., Brill and Bushnell, 1991; Brill et al.,
1998). Interestingly, the metabolic rates of resting yellowtail and rainbow trout
are comparable when corrected for temperature (assuming a Qlo of 2; Boehlert,
1978; Moffitt and Crawshaw, 1983).
A. Oxygen Transport from Water to Tissues
The rate of oxygen movement across the gill respiratory epitbelium is directly
proportional to functional surface area and inversely proportional to the thickness
of the diffusion barrier (Wood and Perry, 1985). Tunas have gill surface areas
approximately seven to nine times larger, and gill blood-water barrier thicknesses
approximately an order of magnitude less, than those of rainbow trout (Table I).
These anatomical adaptations appear to be required for the relatively elevated rate
of gas transfer across tuna gills occurring even at routine activity levels (Hughes,
1984; Perry, 1992). Skipjack and yellowfin tunas have ventilation volumes ap-
proximately 5 to 10 times those of other teleosts (Table I), yet because of their
large thin gills, both are able to extract approximately 50% of the oxygen from
the ventilatory water stream (utilization, Table I). The effectiveness of oxygen
transfer from water (E,) is the ratio of the actual rate of removal of oxygen from
the ventilatory water stream to the theoretically maximum possible rate. E, in
tunas (>60%) is substantially higher than that in trout (33%), indicating that a
larger fraction of the ventilatory water stream is in effective contact with the gas
exchange surface in tunas.
Oxygen diffusing across the lamella is carried away from the gill by red blood
cells. Contrary to much of the speculation in the early literature, the oxygen con-
tent of arterial blood (C,O,) in tunas is not unusual (Bushnell and Brill, 1992;
Korsmeyer et al., 1997b). This is because the elevated hematocrit and hemoglobin
levels reported originally were based on blood samples taken from highly stressed,
recently boated fish (Klawe et al., 1963). Neither are seen in catheterized tunas
that are fully recovered from handling and surgery (Bushnell and Brill, 1992; Brill
and Jones, 1994; Lowe et al., 1998). High rates of oxygen delivery to the tissues
(0, delivery, Table I) at routine activity levels are, therefore, sustained by high
cardiac output (approximately three times those of other teleosts). This, in turn, is
made possible by large stroke volumes, rather than elevated heart rates (when
comparisons are made at equivalent body temperatures). It should be noted,
however, that the cardiac output of rainbow trout has been shown to be linearly
related to acclimation temperature, with a Qlo of ~4 (Barron et al., 1987). When
extrapolated to an acclimation temperature of 25°C (skipjack and yellowfin
tunas’ normal water temperature), the cardiac output of rainbow trout (SO-90 ml
3. THE CARDIOVASCULAR SYSTEM OF TUNAS 85
min-’ kg-‘) could theoretically approach those of tunas. This cardiac output, how-
ever, more likely reflects maximum, rather than routine, outputs in trout (Farrell
et al., 1996).
Elevated cardiac outputs increase the transfer factors (TO,; i.e., the rate of
oxygen transfer from the water to the blood per unit 0, partial pressure difference
between the water and venous blood) of skipjack and yellowfin tunas to approxi-
mately two orders of magnitude above those measured in other fishes (Bushnell
and Brill, 1992). High cardiac outputs also ensure that ventilation and perfusion
capacities in tunas are well matched, since the rate at which oxygen is delivered
to the gills by the ventilatory water stream will be equivalent to the rate oxygen
can be transported away by the blood. To express this more formally, the ventila-
tion perfusion capacity-rate ratio (i.e., the ratio of the oxygen content of the in-
halant water multiplied by the ventilation volume to the oxygen content of arterial
blood multiplied by the cardiac output) is close to the theoretically ideal value of
one (Piiper and Scheid, 1984).
B. High Blood Pressures and the Maintenance of Tissue

Fluid Balance
Skipjack and yellowfin tunas’ high cardiac outputs also generate unusually
high (for a teleost) arterial blood pressures (Table I). Although blood pressure is
the product of cardiac output and total peripheral resistance, the elevated dorsal
and ventral aortic blood pressures of tunas are solely a result of the former, as the
total vascular resistance is actually below that of other fishes (Bushnell et al..
1992). The tunas’ large gills and vascular countercurrent heat exchangers both
contain numerous parallel blood flow channels (Kishinouye, 1923; Muir and
Hughes, 1969; Muir, 1970; Muir and Brown, 197 1; Stevens et al., 1974; Graham
and Diener, 1978) and have large total cross-sectional areas. Therefore, they do
not add significantly to total vascular resistance.
The high arterial blood pressures may, however, have consequences with
respect to tissue fluid balance. Although our understanding of this aspect of
tuna cardiovascular function remains incomplete, recent progress has been made.
Plasma colloid osmotic pressure (COP) works in opposition to capillary hydro-
static pressure to maintain tissue fluid balance. At the arterial end of the capillary,
where capillary hydrostatic pressure exceeds COP, fluid filtration results and there
is transfer of extracellular fluid from the plasma to interstitium. At the venous
end of the capillary, when COP exceeds capillary hydrostatic pressure, fluid reab-
sorption occurs (Friedman, 1976). The net fluid flux during the passage of blood
through capillaries, therefore, depends on arterial blood pressure (the primary de-
terminant of capillary hydrostatic pressure) and permeability of the capillaries to
blood proteins and their concentration (the primary contributors to plasma COP).
Hargens et al. (1974) found protein concentrations in cod (Gadus morhua) and
flounder (Pleuronectes platessa) plasma, interstitial, and peritoneal fluid to be es-

sentially identical and concluded that capillary permeability of fishes was high,
and therefore, effective COP across the capillaries was low. In general, it appears
that if capillary hydrostatic pressure is low, a high COP may not be needed to
ensure adequate fluid reabsorption.
Following this chain of logic, high blood pressure (i.e., capillary hydrostatic
pressure) in tunas could result in elevated rates of net fluid transfer from the cap-
illaries to the interstitium. In mammals, fluid not reabsorbed by the capillaries is
drained from the interstitial space by the lymph system. Fish do not have a lymph
system anatomically identical to that of higher vertebrates, but rather a “second-
ary circulatory system” which appears to play a similar role (Steffensen and Lom-
holt, 1992; Olson, 1996). The vessels of the secondary circulation arise from the
walls of various arteries as arteriolar-sized vessels that coalesce into larger trunks.
Dewar et al. (1994) described vessels of a secondary circulation in the central
vascular heat exchangers of skipjack tuna similar to those seen in other teleosts
(e.g., Chopin et al., 1998). There is no evidence, however, that the secondary
circulation is more developed in tunas than in other teleosts (Brill et al., 1998), as
would be expected if tunas had significantly high rates of net fluid transfer out of
the capillaries.
We have attempted to measure capillary pressures in skipjack and yellowfin
tunas (along with coinvestigators D. R. Jones and J. F. Steffensen), but have not
yet succeeded. Our recent work on the relative capillary permeability and protein
concentrations of plasma and various interstitial fluids of yellowfin tuna, cod, and
rainbow trout, however, suggests tuna capillaries have low protein permeability
(Jones et al., 2000). Figure 1 shows that capillaries of yellowfin tuna are far less
permeable to large molecules (e.g., 40-kDa dextran) than those of the other two
species. In yellowfin tuna, plasma COP is thus maintained during passage through
the capillaries, and net fluid transfer out of the vascular system is not excessive.
As might be expected, Figure 1 also suggests that capillary permeability is in-
versely related to dorsal aorta blood pressure (~7, ~5, and =4 kPa in yellowfin
tuna, rainbow trout, and cod, respectively), and presumably capillary pressure.
Bluefish (Pomatomus saltatrix) have mean ventral aortic blood pressures ap-
proaching those of tunas (a10 kPa; Ogilvy et al., 1988), and a study of their
capillary permeability could be useful to test the hypothesis that the capillary per-
meability and blood pressures are indeed inversely related.
III. MAXIMAL RATES OF CARDIOVASCULAR

FUNCTION IN TUNAS
To take advantage of the resources of the pelagic environment, skipjack,

yellowfin, and bigeye tunas are highly aggregated and highly mobile. Although
500 - kDa dextran
40- kLh dextran
0-j
0 100 200 300 400 500 BOO 700 a 10
Elapsed time (min)
Fig. 1. Plasma concentration of fluorescein-isothiocyanate-labeled dextran (FJTC-dextran) fol-

lowing a bolus injection of the marker into the ventral aorta. The initial rapid drop is most likely a
result of the marker equilibrating within the circulatory system. In yellowfin tuna (open symbols),
dextran molecules as small as 40 kilo-Dahons &Da) remain within the vascular compartment, as
demonstrated by constant plasma concentrations after 200 min. In cod (filled symbols), even with
molecules as large as 500 kDa, plasma concentration continues to decline, indicating a leak from the
vascular compartment, most likely into the interstitial space. Plasma decay curves for rainbow trout
(data not shown) injected with 5OOkDa dextran were similar to those for cod. The data clearly show
the capillaries of yellowtin tuna are less permeable than are those of other teleosts, a characteristic
which is important for maintaining tissue fluid balance in the face of elevated blood pressures (data
from Jones et al., 2000).
the former makes them an exploitable, economically important resource (Sharp,

1978) it is the latter that has shaped much of the thinking about tuna biology. As
a result, there has been a general focus on what initially appeared to be their ex-
ceptional locomotor abilities (e.g., Walters, 1962; Carey, 1973; Graham, 1975;
Magnuson, 1978; Stevens and Carey, 1981; Sharp, 1983; Bushnell and Holland,
1989; Block, 1991). While they are certainly capable of high burst and cruising
speeds, there is little evidence that maximum burst and maximum sustainable
swimming speeds of skipjack and yellowfin tunas are significantly above those of
other active teleosts living at similar temperatures (Brill, 1996). Rather, as first
recognized by Bushnell and Brill ( 1991) and later reinforced by Korsmeyer et al.
(1996a), the cardiovascular systems of skipjack and yellowfin tunas appear ca-
pable of delivering oxygen and metabolic substrates at exceptionally high rates to
meet multiple metabolic demands simultaneously (e.g., rapid lactate metabolism,
rapid digestion, and high growth rates) rather than to allow exceptionally high
sustained swimming speeds. For example, based on data presented in Guppy et al.
(1979), Arthur et al. (1992), Dewar (1993), Brill(1994), and Bushnell and Jones
(1994), during recovery from exhaustive exercise, skipjack tuna swimming at
about 1.5 body lengths s-l would have to reach a total metabolic rate of 2276 mg
O2 kg-* h-l to metabolize white muscle lactate over the observed 2-h time course.
This prediction closely approaches the highest metabolic rate thus far measured
in tunas--=2500 mg 0, kg-’ h- i in skipjack tuna immediately after capture
at sea and which were presumably recovering from exhaustive exercise (Good-
ing et al, 1981). In contrast, the highest metabolic rate of which other teleosts
of approximately equivalent body mass are capable is approximately 1000 mg
0, kg-’ h-’ (Brett, 1972).
A. How Skipjack and Yellowfin Tunas .Achieve High

Maximum Metabolic Rates
Although routine rates of cardiovascular function (Table I) have been quanti-

fied in skipjack and yellowfin tunas with at least some degree of certainty, maxi-
mal rates have not. Rather, they are based on a limited number of observations
(Korsmeyer, 1996; Korsmeyer et al., 1997a,b) and extrapolations (Sri11 and Bush-
nell, 1991; Brill, 1994; Bushnell and Jones, 1994; Korsmeyer et al., 1996a,b).
To date, Graham et al (1989), Dewar and Graham (1994), and Korsmeyer et al.
(1997a,b) are the only investigators to have successfully measured changes in
metabolic rate and cardiovascular function in tunas swimming at various veloci-
ties in a water tunnel. Unfortunately, the range of speeds at which the instru-
mented fish would swim was limited (~0.8-2.4 body lengths s-l), and it remains
unclear if metabolic demand and associated rates of cardiovascular function were
indeed maximal and representative of rates in free-swimming tunas in the wild.
Regardless, the experimental observations and mathematical extrapolations are
now beginning to form a reasonably consistent picture of tunas’ physiological
capabilities.
The relationship between metabolic rate, cardiac output, and blood oxygen-
carrying capacity can be described by three equations,
00, = Q . (Olm,ri,, blood

- COL,us mxx,), (1)
Q = HR . SV, (2)
[O&ax = MCHC HCT . [02 &

where:
VO, is metabolic rate;
Q, cardiac output;
3. THE CARDIOVASCULAR SYSTEM OF TUNAS
[“Zlmenal oxygen content of the arterial blood;

blmxb
[021venous oxygen content of the venous blood;

bloodt
HR, heart rate;

SV, stroke volume;
[Wmax, maximum oxygen-carrying capacity of the arterial blood;
MCHC, mean red blood cell hemoglobin concentration;
HCT, hematocrit; and
[0, nb], oxygen-carrying capacity per unit mass of hemoglobin.
Although tunas could increase any or all of the variables in Equations (l)-(3)
to reach their maximum metabolic rates, they appear to attain high rates of oxygen
and substrate delivery as a result of (a) three anatomical adaptations (large gill
surface area, thin blood-water barrier in the gills, and enlarged ventricle mass:
Table I), (b) the ability to achieve high arterial-venous content difference (Equa-
tions 1 and 3), and (c) the ability to reach exceptionally high maximum cardiac
outputs through high heart rates and large stroke volumes (Equation 2; Brill and
Bushnell, 1991; Bushnell and Jones, 1994; Farrell, 1991, 1996).
The cardiac outputs required to meet tunas’ estimated maximum metabolic
rates, and how these are achieved. are relevant to several other aspects of tuna
biology and therefore we examine these subjects in some detail. Unfortunately,
the maximum cardiac output of any tuna species has never been measured. By
combining available data from a number of sources, however, we can use Equa-
tion (1) to model an upper, physiologically reasonable limit that can be tested in
future experiments. As is clear from Equation (1 ), in addition to knowing maximal
VO,, an estimate of the maximal (]Oallmenarb,ood- [021venous b,ood)is also required.
While this too has never been measured, previous studies give us some insight into
tuna blood oxygen-carrying capacity as well as oxygen extraction potential at the
tissues.
The maximal ([021anelralblood- [021venou5 bl&) will be determined in part by
tmnax> which, in turn, is determined by hematocrit (Equation 3). The normal
hematocrits of skipjack and yellowfin tuna range from 27 to 34% (Bushnell and
Brill, 1992; Korsmeyer et al., 1997b). An hematocrit of ~50% is seen during
recovery from exhaustive exercise (White et al., 1988) due to red cell ejection
from the spleen, red cell swelling, loss of plasma volume, or (more likely) a com-
bination of all three (Yamamoto and Itazawa, 1989). A HCT of 50% and a MCHC
of 370 g liter -I (Korsmeyer et al., 1997b; Lowe et al., 1998) would result in a
blood hemoglobin concentration of 185 g liter-‘, a value within the range of those
measured in tunas recently boated at sea ( 14 I-207 g liter I; Klawe et al., 1963).
At 25°C the oxygen-carrying capacity of hemoglobin is 1.25 ml Oz g ’ (Ganong,
1973) resulting in a maximum predicted ]021anenal h,ocld
of 23 1 ml O? liter -I. It is un-
likely that tuna could produce a [Oz Ivenau5b,cx,d
of zero. The lowest values for skip-
jack and yellowfin tuna reported in the literature are -70-80 ml O2 liter I--
400
arterial-venous 0 2 content difference (ml 0 2 liter -’ blood)
‘.g 250
E
E 200
3
a 150
.-b:
; 100
0
50
0
0 5 10 15 20 25 30 35 40
O2 consumption (ml min-’ kg“)
Fig. 2. Predicted cardiac outputs required to reach various rates of oxygen consumption in skip-
jack and yellowfin tuna as a function of the arterial-venous (A-V) blood oxygen content difference.
At a reasonable maximum A-V blood oxygen content difference (150 ml 0, liter-l blood), estimated
maximum metabolic rates could be achieved by doubling routine cardiac output. Figure is adapted
from Bushnell and Jones (1994); reprinted with permission.
values recorded during severe hypoxia (Bushnell and Brill, 1992) and recovery
from anesthesia (Korsmeyer et al., 1997b). Based on these estimates, maximum
mucteri,, blood - ro*l”e”o”s bhd)in tunas is most likely about 151-161 ml 0,
liter-‘.
By applying these data to Figure 2, in order to generate their maximum docu-
mented metabolic rate (32 ml 0, min.-’ at -25°C; Gooding etaZ., 1981), skipjack
tuna would have to attain a cardiac output of 2 12 ml min- I kg-‘, or an increase of
approximately 1.6 times their routine cardiac output (Table I). The predicted in-
crease in cardiac output is less than that measured by Kiceniuk and Jones (1977)
in freshwater rainbow trout going from rest to maximum sustainable swimming
speed (3 X increase), but it is similar to that observed by Thorarensen et aZ., (1996)
in seawater-acclimated rainbow trout (1.8X increase).
The limited amount of data collected in viva supports the model’s predictions.
For instance, the maximum increases in cardiac output and heart rate in yellowfin
tuna observed by Korsmeyer et al. (1997a) during exercise was approximately
about 1.3 and 1.5 times above those seen in slowly swimming fish. Moreover, the
maximum increase in heart rate observed in swimming yellowfin tuna matches
that seen in nonswimming fish whose vagal control of heart rate has been blocked
by injection of atropine (Keen et al., 1995). Since stroke volume appears to be
3. THE CARDIOVASCULAR SYSTEM OF TUNAS 9 I
fixed in skipjack and yellowfin tunas (discussed in detail in next section), cardiac
output mirrors changes in heart rate. Taken together, both the model and data
suggest that the ratio of maximal to routine cardiac output in tunas is similar to
that of other active teleosts. It should be noted, however, that the predicted maxi-
mum cardiac output of skipjack tuna (>200 ml min-’ kg-’ at 25°C) is still sub-
stantially higher (~3 to 4 times) than those of other fishes (Table I).
B. Elevated Hematocrit, Oxygen Transport, and

Blood Viscosity
The positive impact of high maximum hematocrit (~50% in tunas) on maxi-

mum blood oxygen-carrying capacity can potentially be offset by the resulting
increase in blood viscosity which raises blood pressure, a primary determinant of
cardiac work and maximum cardiac output. As a result, increases in blood vis-
cosity could reduce maximum cardiac output and actually impair blood flow and
oxygen delivery (Egginton, 1998). In tuna (as well as all vertebrates studied to
date), blood viscosity increases exponentially with hematocrit (Figure 3A), while
maximum blood oxygen content increases linearly (Fletcher and Hedrich, 1987;
Wells and Baldwin, 1990). The relationship between the two is reflected in the
blood oxygen transport capacity, which is the quotient of maximum blood oxygen
capacity divided by viscosity. When plotted against hematocrit (Figure 3B), blood
oxygen transport capacity is highly nonlinear, with maximal blood oxygen trans-
port capacity representing the theoretically “optimal” hematocrit.
Interestingly, the increase in viscosity with hematocrit in yellowfin tuna blood
(Figure 3A) is clearly less than that in blood from other fishes (Brill and Jones,
1994). As a result, increases in hematocrit above -30% have little effect on blood
oxygen transport capacity (Figure 3B). The hematocrit likely occurring in yellow-
fin tuna during periods of maximal metabolic rates (-50%) would still, therefore,
be considered “optimal.” Mention should be made, however, that contrary to the
predicted detrimental effects of high viscosity, in viva studies of rainbow trout
show that increases in hematocrit from =30% to over 50% had no effect on maxi-
mum rates of oxygen uptake. The expected decrease in maximum cardiac output
with increase in hematocrit did not occur, and increased blood viscosity actually
had a slight positive effect on maximum sustainable swimming speeds (Gallau-
gher et al., 1995). It is, therefore. an open question if the concept of “optimal
hematocrit” is applicable in viva, and the reason(s) for the unusual behavior of
yellowfin tuna blood remains unexplained.
IV. TUNA CARDIAC FUNCTION
Tuna cardiac anatomy and physiology have been the subject of comprehensive
reviews (Brill and Bushnell, 1991; Farrell, 1991. 1996; Bushnell et al., 1992;
Rainbow trout (15%)
Rainbow trml(15DC)
B
Y
0 lb ;o do 4’0 ;o $0
Hematocrit (%)
Fig. 3. (A) Effects of hematocrit on viscosity of yellowfin tuna blood at 15 and 25°C. and equiva-
lent data for rainbow trout (at 15“C). (The shear rate in both instances was 90 s-l.) (B) Effects of
hematocrit on blood oxygen transport capacity in yellowfin tuna at 15 and 25°C and rainbow trout (at
15°C). The increase in blood viscosity with increasing hematocrit is less steep in yellowfin tuna blood
than in rainbow trout blood. As a result, in yellowfin tuna, increases in hematocrit above 30% have
almost no influence on blood oxygen transport capacity. Figure redrawn from data present in Wells
and Weber ( 199 1) and Brill and Jones ( 1994).
Bushnell and Jones, 1994; Agnisola and Tota, 1994; Moyes, 1996; Tibbits, 1996).
We have, however, chosen to examine this subject in some detail because cardiac
function is central to understanding of cardiovascular physiology and perhaps
even the physiological ecology of tunas (Brill et al., 1999).
As described in Sanchez-Quintana and Hurle (1987) and Farrell and Jones
(1992), tuna ventricles are large (Table I), thick walled, and pyramidal, character-
istics required to produce high ventricular pressures. The inner compact muscle
6) t
3. THE CARDIOVASCULAR SYSTEM OF TUNAS
fibers surrounding the vertices have a coil-like arrangement. The more superticial
compact layer muscle fibers form loops around the ventricle, but with a transverst:
fiber orientation on the caudal face. This fiber morphology is thought to provide
the necessary mechanical advantage for rapid ejection of stroke volume. since the
ventricle can contract simultaneously in the longitudinal and transverse directions.
According to the classification scheme developed by Tota et al. (I 983) and
Tota (1983, 1989), tunas have type IV hearts typical of high-energy-demand te-
leosts-hearts with more than 30% compact myocardium and coronary arteries
in the compact and spongy myocardium. The fraction of ventricular mass com-
posed of compact myocardium is, however, clearly elevated only in bigeye tuna
(>70%) compared to other fishes (- 15-50%; Brill and Bushnell, 1991). The tuna
myocardium is very well vascularized, with highly branched arterioles and ven-
ules, and extensive capillarization which extends even into the spongy myocar-
dium (Tota, 1983). Not surprisingly, tuna hearts may be more dependent on coro-
nary circulation than other teleosts (Farrell et al., 1992). Whereas in other active
fishes an intact coronary circulation is important only during strenuous exercise
or severe hypoxia (Farrell and Steffensen, 1987), in vitro experiments have shown
that skipjack tuna hearts depend on an intact coronary circulation for normal func-
tion (Farrell et al., 1992). This presumably is also the case in viva As expected,
the estimated coronary blood flow rate (ml blood go-’ ventricle min ‘) is approxi-
mately twice as great in skipjack tuna hearts as in those of rainbow trout (Farrell.
1996). No work has been conducted on factors controlling coronary blood flow
in tunas.
A. Stroke Volume
The routine stroke volume of skipjack and yellowfin tuna hearts (- 1 ml kg -‘)
approaches the maximum stroke volume of other fishes (Table I). More impor-
tantly, however, both in viva and in vitro data suggest that tuna hearts normally
function at close to their maximum stroke volumes. In other words, unlike hearts
of other teleosts, tuna ventricles appear to have a very limited ability to increase
stroke volume. This was first noted during experiments to quantify hypoxia tol-
erance. Bushnell et al. (1990) and Bushnell and Brill(1992) found hypoxic brady-
cardia occurring in skipjack and yellowfin tunas to be accompanied by nearly
equivalent reductions in cardiac output. In other fishes (e.g., cod and lingcod
Ophiodon elongatus) hypoxic bradycardia is accompanied by compensatory in-
creases in stroke volume sufficient to maintain cardiac output (Farrell, 1982; Frit-
sche and Nilsson, 1989). Yellowfin and skipjack tunas’ limited ability to increase
stroke volume is also observed in fish subjected to acute reductions in ambient
temperature (from 25 to = 18°C; Korsmeyer et al., 1997a; R. Brill, K. Cousins,
and T. Lowe, unpublished observations). Under these conditions too, decreases in
heart rate result in nearly parallel reductions in cardiac output because of only
modest (- 15%) increases in stroke volume. In contrast, when porgy (Pagrus ma-
jor) are subjected to a similar acute reduction in ambient temperature, the fall in
heart rate is accompanied by an increase in stroke volume sufficient to maintain
cardiac output (Azuma et al., 1998). This compensatory response to acute tem-
perature changes is not universal, however. Although hypoxic bradycardia in ling-
cod results in increased stroke volume, bradycardia accompanying acute reduc-
tions in ambient temperatures does not, and cardiac output decreases in almost
direct proportion to heart rate (Stevens et al., 1972).
The limited ability of tunas to elevate stroke volume in viva is also apparent
during forced activity. While elevated activity levels in yellowfin tuna result in
increases in cardiac output (Korsmeyer et al., 1997a,b), as they do in other teleosts
(Farrell and Jones, 1992), increases in cardiac output are accomplished solely by
increases in heart rate with no measurable change in stroke volume (Figure 4A).
In contrast, rainbow trout increase cardiac output during exercise by doubling
stroke volume and only fractionally changing heart rate (Figure 4B). In general,
in teleosts other than tunas, =40-60% of the increase in cardiac output during
exercise is due to a rise in stroke volume, with the remainder due to elevations in
heart rate (Farrell, 1991).
The tuna heart’s limited ability to increase stroke volume can also be demon-
strated in vitro. In fish hearts, as in mammalian hearts, there is a positive cor-
relation between end diastolic ventricular volume (preload) and stroke volume
(Farrell, 1984). The phenomenon is intrinsic to the myocardium (Harwood et al.,
1999) and is referred to as the “Frank-Starling mechanism,” after its discoverers.
In vitro, end diastolic ventricular volume is altered by changing ventricular filling
pressure, and the resultant relationship of ventricular filling pressure to stroke
volume is referred to as a “Starling curve.” Examples from several teleosts are
shown in Figure 5. Note that the Starling curve for skipjack tuna ventricles has
the same shape as those for other fishes, but only at subambient filling pressures.
Unfortunately, with skipjack tuna hearts in vitro, raising filling pressures above
ambient results in ventricular failure, possibly due to the inability to adequately
perfuse the coronary circulation in these circumstances (Farrell et al., 1992). Lai
et al. (1987) have reported subambient pericardial pressures in albacore, although
these were subsequently not observed in yellowfin tuna (Jones et al., 1993). Re-
gardless of these inconsistencies, it is important to appreciate the fact that over
the range of input pressures needed to produce near-routine stroke volume
(- 1 ml kg-‘), stroke volume appears almost insensitive to filling pressure (i.e., to
end diastolic ventricular volume) in skipjack tuna hearts. We surmise that, in gen-
eral, both skipjack and yellowfin tuna hearts normally function on the upper flat
portion of their Starling curve where stroke volume is insensitive to preload filling
pressure or filling time (i.e., cardiac interval). Other teleost hearts function on the
“steeper” parts of their Starling curves (Figure 5).
+ heart rate
1.6 - f- stroke volume
+ cardiac output
8 1.4 .
ii Yellowfin tuna
5
1.5 2.0 2.5

Swimming speed (relative change)
+ heart rate B
- Stroke volume
3.0 4 cardiac output
0 20 80 100
SwimnZg speed6y%Uctit)
Fig. 4. Effect of swimming speed on the relative change in cardiac output, heart rate, and stoke
volume in a yellowfin tuna (A) and rainbow trout (B). Note that in yellowfin tuna increases in cardiac
output are accomplished by increases in heart rate alone, whereas in rainbow trout both heart rate and
stoke volume increase with increases in swimming speed. Data for yellowfin tuna are from Korsmeyer
et al. (1997a), and those for rainbow trout from Kiceniuk and Jones (1977).
B. Maximal Heart Rates in Tunas and Other Teleosts
Because maximum heart rates in fishes are temperature labile, comparisons of

maximum heart rates in tunas to those of other species are somewhat difficult. In
general, the maximum heart rate of teleosts has been reported to be 120 beats
min-’ (Farrell, 1991), even at temperatures as high as 35°C (Gehrke and Fielder,
1988). The maximum heart rates of skipjack tuna (-200 beats min-‘; Kanwisher
et al., 1974; Keen et al., 1995) have, therefore, been considered to be the highest
96 RICHARD W. BRfLL AND PETER G. BUSHNELL
Skipjack tuna,
1
T
'UJ
x o.a-
E.
!i 0.6-
2
P
d 0.4-
g
co
0.2-
I
I I I I I I I I
-0.266 -0.133 0 0.133 0.266
Ventricular filling pressure (kPa)
Fig. 5. Effects of filling pressure on cardiac stroke volume (i.e., Starling curves) of isolated
perfused hearts from several species of teleosts. With the exception of tunas, teleost hearts normally
operate over the steep portion of their Starling curves. Tuna hearts, however, normally operate at
nearly maximum stroke volumes (i.e., at positive ventricular filling pressures where the Starling curves
are relatively flat). Figure is from Farrell (1991); reprinted with permission.
among teleosts. This may no longer strictly be the case since a tropical tide pool
goby, Bathygobius soporator, has now been reported to have maximum heart rates
of 225 beats min-’ (at 35°C; Rantin et al., 1998).
In addition to having heart rates that are generally higher than most other te-
leosts, there are also clear differences in the neural control of heart rate in tunas.
The intrinsic activity of the teleost heart’s pacemaker cells can be influenced by
several factors, including temperature, adrenergic stimulation, and cholinergic
stimulation (Farrell and Jones, 1992). Tunas are unusual among teleosts in that
cholinergic inhibitory tone (via the vagus nerve) is the predominate controller of
heart rate. Blocking vagal activity with atropine causes a 58% (75 to 120 beats
mm’) and 143% (79 to 193 beats min-‘) increase in heart rate in yellowfin and
skipjack tunas, respectively (Keen et al., 1995). In other teleosts (excluding the
antarctic icefishes, Pugothenia spp.), the same treatment generally results in less
than a 30% increase in heart rate (Farrell and Jones, 1992). Adrenergic blocking
agents in tunas have minimal influence on resting heart rates (Keen et al., 1995),
and clearly less than that seen in other teleosts (Farrell and Jones, 1992). The
predominant vagal control of heart rate in tunas begs the question, “What (if any)
is the role of sympathetic, adrenergic stimulation on routine or maximum heart
rates of tunas?” Injection of a sympathomimetic, epinephrine, is vasoactive and
can increase ventral aortic blood pressure (to >25 kPa), heart rate, and cardiac
output in skipjack and yellowfin tunas, although none of these effects have been
quantitatively investigated (Bushnell and Brill, unpublished observations). To our
knowledge the sympathetic system’s influence on blood flow distribution to vari-
ous vascular beds in tunas remains unstudied.
In spite of a fixed stroke volume, the skipjack tuna’s high heart rate can eas-
ily accommodate its documented maximum metabolic demand. As shown in
Figure 6, assuming no increase in stroke volume, maximum heart rate (~200
beats min-‘) is more than sufficient to account for the cardiac output (212 ml
min- ’ kg-‘; Figure 2) accompanying the estimated maximum metabolic rate. Also
as shown in Figure 6, this is in direct contrast to observed changes with exercise
occurring in trout, where increased cardiac output is accomplished by increases in
both stroke volume and heart rate.
3 160 -
I
.E
E
2 120.
8
e 240
g 80.
2
I
I 40-
-------- .. . .
oc
0.0 0.3 0.6 0.9 1.2 1.5 1.8 2.1
I
2.4
Stroke volume (ml kg-‘)
Fig. 6. Relationship of heart rate, stroke volume, and cardiac output in freshwater (Trout,)- and
seawater (Trot&.)-adapted rainbow trout, yellowtail, yellowtin tuna, and skipjack tuna. Filled circles
show minimal values, and open circles maximal values. In fish other than tunas, increases in cardiac
output accompanying increases in activity are accomplished primarily by increases in stoke volume
(Trout,) or approximately equal increases in stoke volume and heart rate (TroutsW). In contrast, the
predicted cardiac output (>200 ml mm ’ kg ‘) required to meet skipjack tuna’s observed maximum
metabolic rates can be met by maximum observed heart rates, with no increase in stroke volume. Data
for freshwater-adapted trout are from Kiceniuk and Jones (1977), seawater-adapted trout from Thor-
arensen er al. (1996), yellowtail from Ishimatsu rr al. (1997). and skipjack and yellowfin tuna from
Bushnell and Brill (1992).
C. Sarcoplasmic Reticulum
A key factor influencing rates of ventricular contraction and relaxation is the

cycling of calcium ions (Caz+) into and out of the cardiac muscle cells (myocytes).
In mammalian myocardium, Ca*+ influx is initiated through sarcolemmal voltage-
gated Ca*+ channels which serve to trigger a larger Ca2+ release from the sarco-
plasmic reticulum (SR). This process is referred to as “Ca*+-induced Ca2+ re-
lease” (Fabiato, 1983). Since SR-Ca2+ stores are intracellular, diffusion distances
are relatively short, and the time course of Ca*+ release and resequestering can be
rapid. When myocyte volumes are small relative to their surface areas, however,
a well-developed SR may not be necessary. As a consequence of a high ratio of
sarcolemmal (i.e., cell surface) area to myocyte volume, extracellular Ca2+ alone
can be sufficient to initiate myofibrillar contraction (Tibbits et al., 1992b). Ana-
tomical studies tend to support this idea. Fish myocyte diameters range from ap-
proximately 2 to 10 Frn, compared with 10 to 25 pm in mammals (Santer, 1985;
Satchel& 1991), and the SR in teleost hearts is generally considered to be not well
developed (Yamamoto, 1967; Santer, 1974; Breisch et al., 1983; Satchell, 1991).
Myocyte diameters in albacore, the only tuna species from which we currently
have data, range from 2.5 to 6 ,um and therefore are not unique in this regard
(Breisch et al., 1983).
Although there are some species-specific differences in the extent of SR de-
velopment among the teleosts, it is unclear if SR volume is related to general
activity level as might be expected. For example, electron micrograph studies by
Yamamoto (1967) and Santer (1974) indicate that the SR is less extensive in the
ventricle of goldfish (Curussius uurutus) than in that of the more active rainbow
trout. In contrast, Breisch et al. (1983) stated that in albacore, “the sarcoplasmic
reticulum, although present, is very poorly developed.” More recently, prelimi-
nary studies (K. L. Cousins, unpublished observations) suggest that the yellowfin
tuna ventricle (Figure 7) has a SR at least as well developed as that of rainbow
trout or carp (Cyprinus cur@), but all are clearly less developed than the rat’s
(Santer, 1974; Chugun et al., 1999). Electron microscopy quantitatively compar-
ing the development of the SR in skipjack tuna, yellowfin tuna, the ectothermic
scombrids, and several other fish (including those of different activity levels)
seems clearly warranted.
While anatomical studies can be used to establish the distribution and devel-
opment of SR, accompanying physiological studies on the importance of SR-
derived Ca*+ in initiating contraction are required. The latter involve the use of
ryanodine, which, at high concentrations, locks the SR Ca2+-gated Ca2+-release
channel in a subconducting state, making the SR ineffective with respect to Ca2+
release or sequestering (Rousseau et al., 1987). Decreases in peak tension devel-
oped by isolated atria1 or ventricular strips exposed to ryanodine can be used to
assess the relative contribution of extracellular (sarcolemmal)- and SR-derived
Fig. 7. Transmission electron micrograph of yellowfin tuna ventricle (compact myocardium)

with myofibers cut in transverse section (original magnification 15900X). Although sarcoplasmic
reticulum (SR) is clearly evident, pending a careful quantitative study, it remains an open question if
the SR is more developed in tuna myocardium than in the hearts of other active teleosts (K. Cousins.
unpublished observations). Mi indicates mitochondria, Mf myofilaments.
Ca2+. These types of studies have shown that SR-Ca*+ release in teleosts myocar-
dium is negligible except in nonphysiological circumstances such as supraphy-
siological temperatures or subphysiological pacing frequencies (Tibbits et al.,
1992b; Keen et al., 1994; Gesser, 1996; Shiels and Farrell, 1997). In contrast,
Keen et al. (1992) and Shiels et al. (1999) demonstrated that in skipjack and yel-
lowfin tuna atria1 strips, SR-Ca*+ release contributes ~30% and ~60% (respec-
tively) of activator Ca2+ under normal operating temperatures (15 -25°C) and pac-
ing frequencies (up to 2.5 Hz).
lnterpretation of these findings is somewhat obfuscated by the apparent, tem-
perature sensitivity of the ryanodine response. Hove-Madsen (1992) found that
the ryanodine sensitivity of rainbow trout myocardium was negligible at 15°C.
Skipjack tuna (25%)
0.0 0.5 1.0 1.5 2.0 2.5 3.0 3.5

Stimubtbn frequency (Hz)
Fig. 8. Contribution of SR-CaZ+ release to force development in isolated myocardial strips from
yellowfin tuna at 15, 18, and 25°C (from Shiels et al., 1999) and from skipjack tuna at 25°C (from
Keen ef aZ., 1992). Data are presented as the fractional reductions in force resulting from exposure to
ryanodine. Error bars have been omitted for clarity. Note that contribution of SR-derived Caz+ is less
in skipjack tuna than in yellowfin tuna myocardial strips. The contribution of SR-derived Ca*+ is
greater at lower temperatures in yellowfin tuna, which is in direct contrast to results from other teleosts.
In rainbow trout myocardiom, the importance of SR-derived Ca *+ is greater at higher temperatures.
while at 25°C SR-Ca2+ release accounted for 40% of activator Ca*+. The lack of
ryanodine sensitivity at 15°C most likely results from locking the SR-Ca2+ release
channel in the open position (Tibbits, 1996). In contrast, the temperature sensi-
tivity of ryanodine response in tuna hearts appears to be exactly the opposite, as
Shiels et al. (1999) found yellowfin tuna atrial strips to have a greater ryanodine
sensitivity at 15°C than at 25°C (Figure 8). The implied fundamental differences
between SR-Ca*+ release channels in tuna and those in other teleosts are obviously
another avenue that needs to be explored, perhaps at the molecular level (e.g.,
Tibbits et al., 1992a).
Temperature effects not withstanding, there appear to be substantial differ-
ences in the importance of SR-Ca2+ release just within tuna species. Shiels et al.
(1999) found a greater importance of SR-Ca2+ release in atrial strips from yellow-
fin tuna (~60%; Figure 8) than in those from skipjack tuna (~30%) studied by
Keen et al. (1995). Given the differences in maximum heart rates of yellowfin
(120-140 beats mini) and skipjack (-200 beats mini) tunas, the opposite rela-
tive SR-Ca*+ contributions would be predicted as higher maximum heart rates
should be more dependent on SR-Ca2+ release and resequestering (Farrell, 1996).
It is possible that these findings may result from different techniques; Shiels et al.
(1999) used 1 nM adrenaline in their tissue bathing medium whereas Keen et al.
(1995) did not. If in tuna myocardium adrenaline is required to enhance extracel-
lular Ca2+ release enough so as to fully stimulate SR-Ca2+ release, then its absence
may cause the contribution SR-Ca2+ release to be underestimated. Freund (1999),
however, also found that increasing extracellular Ca2+ has no effect on force of
contraction of ventricular strips from yellowfin tuna at high pacing frequencies,
as it does in atrial strips from skipjack tuna (Keen et al., 1992) and cod (Driedzic
and Gesser, 1985). These data also indicate a larger dependence on SR-CaZ+ re-
lease in yellowfin tuna than in skipjack tuna myocardium. A dependence on SR-
Ca2+ may, however, not be strictly necessary for high maximum heart rates.
SR-Ca2+ release and resequestering do not appear to be important in the tide pool
goby (Buthygobius soporutor) even though maximum heart rates in this species
exceed 225 beats mm’. The functioning of ventricular strips isolated from this
species are nearly insensitive to ryanodine (Rantin et al., 1998).
A second method of evaluating SR-Ca*+ release is postrest potentiation, a
technique that monitors the increase in twitch tension of isolated myocardial strips
following a single 20-s “rest” period between twitches (Driedzic and Gesser,
1988). Freund (1999) has recently used this procedure to demonstrate that ven-
tricular strips of Pacific mackerel (Scomber japonicus) are equally dependent on
SR-Ca2+ release as those of yellowfin tuna. These data imply that some of the
unusual characteristics of SR-CaZ+ release channels may have developed early in
scombrid evolution, as they are appear to be present in even primitive members of
the family Scombridue. Shiels and Farm11 (2ooO), however, also using ventricular
trabeculae from Pacific mackerel, found ryanodine induced significantly smaller
(20%) reductions in peak tension than those observed in similarly treated tuna
myocardium. To the best of our knowledge, there are no data on routine or maxi-
mal cardiac function in mackerel, so these observations are yet to be put in an in
viva physiological context. Moreover, mammal&n atria1 muscle shows a greater
ryanodine sensitivity than ventricular muscle (Bers, 1991). If the same occurs in
teleosts, conclusions based on the various studies could be compromised, as some
investigators have used atrial muscle and others ventricular muscle. A compara-
tive study of ryanodine sensitivity of tunas, ectothermic scombrids, and other te-
leosts using the same methodology throughout is clearly needed.
D. Mechanical and Electrical Coupling of Myocytes
The high maximum heart rates of skipjack and yellowfin tunas require that
all links in the chain of excitation-contraction coupling be enhanced (Satchell,
199 1). For example, the short Ca?* diffusion distances from the SR to the myofi-
brils require the depolarization triggering Ca*+ release from the pacemaker tissue
to spread around the ventricle with equal rapidity. Small myocyte diameters, how-
ever, can result in high electrical resistance and slow conduction velocities (Farrell
and Jones, 1992). Since the rate of increase in ventricular pressure (dp/dt) in yel-
low fin tuna hearts in vivo is rapid (up to 7 16 kPa s-l) and in the mammalian range
(Jones et al., 1993), we conclude that there is indeed near-synchronous contrac-
tion of the myocytes. This, in turn, implies the presence of fast conducting fibers
analogous to the bundle of His and Purkinje fibers of mammalian hearts. Al-
though such fibers have not been described histologically in any fish species,
based on the pathways over which depolarization is known to spread across teleost
ventricles, Satchel1 (1991) concluded that fast conducting fibers “certainly oc-
cur.” We would not be surprised to find that specialized fast-conducting fibers are
especially well developed in tuna cardiac muscle, and encourage investigation in
this area.
In addition to rapid electrical conduction from the pacemaker, cells of the
cardiac tissue require both mechanical and electrical coupling. Mechanical cou-
pling of myocytes is accomplished via intercalated disks consisting of fasciae
adherentes (where actin filaments of adjacent myocytes insert onto a dense fibrous
mat) separated by desmosomes (regions of the cell surface specialized for main-
taining cell-to-cell cohesion; Bloom and Fawcett, 1975). Intercalated disks are
present in the hearts of all vertebrates and are clearly present in albacore (Breisch
et al., 1983) and yellowfin tuna (Figure 9). Electrical coupling between myocytes
Fig. 9. Transmission electron micrograph of yellowfin tuna ventricle (compact myocardium)

with myofibers cut in longitudinal section (original magnification 12,500X). Desmosomes, interca-
lated disk, and gap junction are shown. Note that, as in mammalian myocardium, gap junctions appear
to be part of the intercalated disk. Mi indicates mitochondria, Mf myofilaments (K. Cousins, unpub-
lished observations).
occurs through gap junctions (also referred to as nexus junctions) which have been
reported to occur on the lateral walls of adjacent myocytes in several fish species,
including albacore (Shibiata and Yamamoto, 1977; Breisch et al., 1983). As can
be seen in Figure 9, gap junctions are also present in the compact myocardium of
yellowfin tuna and appear to be part of the intercalated disk, as they are in mam-
malian hearts (Bloom and Fawcett, 1975; Satchell, 1991). Cobb (1974) has re-
ported that in fishes, gap junctions are not associated with the fasciae adherentes
of the intercalated disks, but are only on the lateral wall of the myocytes. The
physiological implications of the unusual gap junction distribution in yellowfin
tuna await further investigation. As with the SR, a quantitative morphological
study of gap junctions and intercalated disks involving several species of tunas,
ectothermic scombrids, and other teleosts is clearly needed to discern if the ability
of tunas to reach high maximum heart rates or cardiac outputs is correlated with
more extensive development of these structures.
E. Biochemical Adaptations of Tuna Hearts for

High Power Output
Skipjack and yellowfin tunas’ high cardiac outputs and ventral aortic blood
pressures result in routine cardiac power outputs (per unit body mass) that are
approximately seven times those of other teleosts (Table I). Due to their enlarged
ventricles, however, power output per gram ventricular mass is only twice that
seen in other fishes (Table I). In other words, tunas’ elevated cardiac power out-
puts are achieved primarily through ventricular hyperplasia (Moyes et al., 1992;
Farrell, 1996; Tibbits, 1996).
As expected, the levels of aerobic enzyme activity (citrate synthase and
3-hydroxy-o-acyl-CoA dehydrogenase) per gram ventricle mass are likewise all
roughly double in tuna hearts compared with hearts of other teleosts (Dried&,
1992; Moyes et al., 1992; Dried& and Gesser, 1994; Dickson, 1995). The excep-
tion is camitine-palmitoyl transferase, an enzyme involved in fatty acid metabo-
lism, whose activity is approximately three to seven times higher (Moyes et al.,
1992; Dickson, 1995). Tuna hearts, therefore, appear to rely more on fatty acids
to power aerobic metabolism than do other teleost hearts (Moyes, 1996; Weber
and Haman, 1996). The advantages of fatty acids over glucose as a fuel source are
their higher energy content (i.e., moles of ATP derived per gram of substrate) and
their ability to be stored in the tissues at high levels. It is also possible that tuna
hearts may use lactate as a fuel source, as mitochondria isolated from skipjack
tuna ventricle have a higher capacity for lactate oxidation than other metabolic
fuels (Moyes et al., 1992). This finding makes intuitive sense since the highest
heart rates and cardiac outputs (i.e., highest rates of cardiac energy demand) are
likely to occur in tunas during recovery from exhaustive exercise, when plasma
lactate levels are elevated (Arthur et al., 1992).
The use of lactate as a metabolic energy source in the heart is also supported
by microanatomical differences which reflect metabolic zonation of compact and

spongy myocardium. In albacore, the volume percentage of mitochondria is
higher in the spongy layer (3 1.9%) than in the outer compact myocardium (21.3%;
Breisch et al., 1983). While Basile et aZ. (1976) found mitochondrial volume den-
sities (28-32%) in bluefin tuna (Thunnus thynnus) hearts to be similar to those of
albacore hearts, they did not find differences in mitochondrial volume density
between myocardial layers. They did note, however, that the mitochondria from
the spongy myocardium had higher cristae density. These anatomical findings
support the biochemical observations that the spongy layer has a substantial ca-
pacity to oxidize lactate and incorporate it into lipids for possible use by the com-
pact myocardium (Maresca et al., 1976; Gemelli et al., 1980). This implies the
possibility of metabolic interactions between the two myocardial layers
Cardiac mitochondrial ATP production capacity can serve as another estimate
of cardiac energy demand. As stated earlier, maximum oxygen consumption in
skipjack tunas appears to be met by a doubling of cardiac output (Figure 2). In
yellowfin tuna (the only species in which this has been measured), there is only a
relatively small (>20%) increase in ventral aortic pressure with increasing activity
(Korsmeyer et al., 1997a,b). If the same occurs in skipjack tuna, then maximum
cardiac power output (per gram ventricle) would be ~2 times routine levels, and
= 1.5 -2.5 times those of other teleosts (Table I). It is not unreasonable to expect
that the increase in power output would have to be generated by increases in mi-
tochondrial (i.e., aerobic) ATP production. Studies by Moyes et al. (1992) provide
evidence that the metabolic support does indeed exist, as the maximal mitochon-
drial oxygen consumption of skipjack tuna hearts (7 /.LM 0, g-’ ventricle min-‘)
is approximately twice the estimated routine consumption rate (3.3 PM 0, g-l
ventricle min-I). This level of oxygen consumption is also about twice that of
mitochondria isolated from carp ventricle (per milligram of mitochondrial pro-
tein), when corrected for differences in measurement temperature. These data are
thus reasonably consistent.
The high maximum power output of tuna hearts may also be supported by the
high levels of myoglobin found in tuna ventricles, although exact mechanisms
remain unknown. Giovane et al. (1980) reported ventricular myoglobin levels in
bluefin tuna to be 6-20 mg g-l, a level whose upper range is several times those
of other active teleosts (al-6 mg g-l; Driedzic, 1983). Driedzic (1983,1988) has
suggested that high ventricular myoglobin levels serve to maintain contractility
during episodes of low ambient oxygen. Stevens (1982), however, found that in
fish skeletal muscle, elevated myoglobin levels function to facilitate oxygen dif-
fusion from the capillaries to the mitochondria, rather than as an oxygen store
utilized during hypoxia. A third possibility, put forth by Tota (1983), is that myo-
globin may function as a temporary oxygen store to offset the effects of the brief
periods of ischemia occurring during ventricular contraction when coronary blood
how is likely to be diminished.
F. Ventricular and Arterial Dynamics and Functions of the

Bulbus Arteriosus
While most of the foregoing discussion has concentrated on how the cardio-
respiratory system of tunas achieves high levels of performance, it also important
to note that on a second-to-second basis, cardiovascular function involves highly
dynamic processes. In this regard, based on tunas’ high maximum heart rate it is
possible that the complex hemodynamic relationships seen in birds and mammals
could be present in the circulatory system of tunas. High heart rates result in short
pressure wavelengths, such that length of the arterial tree becomes a significant
proportion of the pressure wavelength (Langille et al., 1983; Jones, 1991). As a
result, the transmission time of the pressure pulse through the arteries can span a
significant portion of the cardiac cycle. In these circumstances, the arterial tree of
tunas would not act as a simple elastic reservoir as it does in other fishes (the so-
called “Windkessel model”). Rather it would behave as it does in mammals as a
wave transmission system with complex wave propagation effects such as pulse
amplification, distortion, and wave reflections. Jones et al. (1993), however, found
no evidence of wave transmission in yellowfin tuna. Rather, pressure and flow
waveforms agreed well with theoretical and mathematical Windkessel models.
This interesting finding probably results from the functional properties of the bul-
bus arteriosus, the highly distensible fourth chamber of the teleost heart. In tunas,
as in other teleosts, the bulbus arteriosus is capable of stretching to accept an
entire stroke volume and recoiling elastically. It thus smooths blood flow pulsatil-
ity and maintains blood flow through the gills during diastole (see Figure 5 in
Bushnell et al., 1992), which presumably improves gas exchange (Malte, 1992).
In contrast, blood flow in the mammalian proximal aorta is highly puisatile, and
often reverses (i.e., momentarily flows backward into the heart) during diastole.
The extreme extensibility of the bulbus arteriosus of yellowfin tuna and alba-
core is shown in Figure 10A as quasi-static pressure-volume loops and demon-
strates how the bulbus arteriosus in tuna is able to maintain blood flow through
the gills during diastole (Jones et ul., 1993). The initial portion of the compliance
curve is very steep (i.e., the bulbus arteriosus is very “stiff” or not very compli-
ant) and pressures remain high even at volumes as low as 10% of maximum in-
jected volume. In vivo, this means that during diastole, when the bulbus arteriosus
is recoiling, ventral aortic pressure remains elevated until nearly the entire stroke
volume has been ejected. This behavior, in turn, provides the motive force to
maintain continuous blood flow through the gills between heartbeats. As is the
case with most teleosts (Bushnell et al., 1992), the yellowfin tuna bulbus arterio-
sus is most compliant (i.e., shows relative small increases in pressure with equal
increments of inflation) over the range of routine ventral aortic blood pressures
(10.8-l 1.8 kPa, Table I). The plateau phase of the quasi-static pressure-volume
loop, therefore, corresponds to ventral aortic systolic pressure. In albacore, how-
ever, the bulbus arteriosus appears to be most compliant at pressures below ventral
aortic blood pressure (10-l 1 kPa; Lai et al., 1987). This result may be somewhat
misleading, as blood pressures in albacore were measured on recently boated fish
and may have been elevated due to stress. If the compliance characteristics of the
bulbus arteriosus are indeed matched to cardiovascular pressures, we would pre-
dict that the ventral aortic pressure of unstressed albacore probably lies in the
range of 6 - 8 kPa. We believe the bulbus arteriosus compliance and ventral blood
pressure relationship may provide researchers with an in vitro experimental tool
that can be used to estimate ventral pressures in species which are not amenable
to laboratory manipulations because of their size or availability We therefore also
present in Figure 1OB a series of pressure-volume loops for the bulbi arteriosi
from a number of pelagic fishes whose blood pressures have yet to be measured.
The data imply that striped marlin (Tetrupturus U&X), blue marlin (Mukairu
nigricuns), and sailfish (Zstiophorus platy~tents) all have blood pressures in the
ventral aorta between those of yellowfin tuna and albacore, whereas those of ma-
himahi (dolphinfish, Coryphuenu hippurus) and pomfret (Tuructichthys spp.) are
clearly lower.
The highly specialized bulbus arteriosus of tunas most likely performs another
very important function: it increases the efficiency of the circulatory system (i.e.,
the ratio of external cardiac work to cardiac energy demand). The majority of
cardiac energy is used to develop systolic blood pressures in the ventricle (i.e., to
develop wall tension; Jones, 1991). Therefore, anything that reduces peak systolic
pressures, or the time over which they must be generated (i.e., the time-tension
index), will reduce cardiac energy demand and thus improve efficiency. Because
of the high heart rates, cardiac outputs, and ventral aortic pressures in tunas, ad-
aptations which reduce the myocardial time-tension index should be expected.
Mathematical modeling studies have shown that a large, central (rather than pe-
ripheral) compliance in the circulatory system is of hemodynamic value as it
raises diastolic pressure while effectively lowering peak systole pressures and,
thus, the time-tension index of the heart (Campbell et al., 198 1). For tunas, which
put exceptional demands on their cardiovascular systems (Table I), the energy
savings due to the presence of a highly compliant bulbus arteriosus are most likely
substantial.
There is, however, a potential problem with having a compliant structure ca-
pable of large changes in volume immediately outside the heart. It would remove
the ability to regulate blood pressure (beat-to-beat) in an effective manner because
any increases in peripheral resistance (or cardiac output), which would normally
cause blood pressure to rise, would be damped by the plateau phase of the bulbus
arteriosus pressure-volume curve (Figure 10). The solution to the problem lies in
having a structure with variable and regulated mechanical properties. This is ac-
complished by having smooth muscle in the walls of the bulbus arteriosus that is
capable of contracting in certain circumstances (Farrell, 1979; Watson and Cobb,
3. THE CARDIOVASCLnAR SYSTEM OF TUNAS 107
16
I + Albacore
14
12
20 40 60 80 100
% of maximum injected volume
Fig. 10. (A) Pressure-volume loops recorded in isolated bulbi arteriosi taken from yellowfin tuna
and albacore. The curves were generated by stepwise injection of measured volumes of saline into
isolated sealed vessels, followed by stepwise removal. The pressure-volume curves created during
inflation are below those created during deflation. (B) Pressure-volume loops recorded in isolated
bulbi arteriosi taken from various pelagic fishes. Based on the tuna data, it is possible that the plateau
region of curves shows the normal ventral aortic blood pressures of these fishes. Data from M. Braun,
University of British Columbia: reprinted with permission.
1979). Not surprisingly, the bulbus arteriosus of tunas is highly vascular, is well
enervated, and possesses significant amounts of smooth muscle (Braun et ul.,
2000). Presumably, contracting or relaxing this smooth muscle allows subtle ma-
nipulation of wall properties and the short-term blood pressure changes necessary
to maintain proper function of the cardiovascular system. The regulation of the
compliance of the tuna bulbus arteriosus is unstudied, but clearly deserves further
investigation.
V. CARDIAC FUNCTION AND THE

PHYSIOLOGICAL ECOLOGY OF TUNAS-
A POSSIBLE CONNECTION
In the following section we consider how the cardiorespiratory physiology of

tunas might impact their behavior and distribution in the open ocean. The ability
to apply what we have learned in the laboratory to what we believe is happening
in the field is possible because of ultrasonic telemetry and new archival tags (i.e.,
electronic data recording devices carried by the fish). These allow detailed records
to be obtained of the horizontal and vertical movements of tunas and other pelagic
fishes in the open sea.
The vertical movements of large adult (~50 kg) and even juvenile (~4-6 kg)
bigeye tuna are much deeper, and into much colder water, than those of yellowfin
tuna (Figure 11). Adult bigeye tuna routinely reach maximum depths of 450-
500 m during the day while juvenile fish are commonly found at 350 m (Holland
et al., 1990b; Boggs, 1992; R. Brill, M. Musyl, D. Cut-ran, and C. Boggs, unpub-
lished observations). The water temperatures at these depths are =5-7°C and
= 15” C, respectively. Ultrasonic tracking studies of large (>25 kg) bigeye tuna near
Tahiti show that they follow the daily vertical migrations of the small nektonic or-
ganisms (crustaceans, cephalopods, and fishes) of the deep sound-scattering layer
even as they descend into deeper and colder water (Josse et al., 1998; Dagorn
et al., 2000). Bigeye tuna thus have the ability to exploit a prey source which,
during daylight hours, apparently is not normally available to yellowfin tuna
(Grundin, 1989; Roger, 1994; Marchal and Lebourges, 1996).
While there are clear instances where the depth distribution of tunas is set by
the depth distribution of their prey (e.g., Block et aE., 1997; Marcinek et al., 2001),
the dichotomous depth distributions of yellowfin and bigeye tunas in exactly the
same area near the main Hawaiian Islands (Figure 11) implies that one or more
abiotic factors are having an impact on their vertical movements. It is possible that
changes in oxygen levels in the water column may be limiting their distribution,
but near the main Hawaiian Islands significant decreases in ambient oxygen do
not occur in the portion of the water column occupied by yellowfin and juvenile
bigeye tunas (Brill et uZ., 1999). We suggest, as first noted by Brill ef al. (1993,
1999), that a major limiting factor is the relative change in water temperature
occurring between the surface layer and the waters below the thermocline. We
believe this to be the case because of the documented effect of acute reductions in
ambient temperature on cardiac function. Since tunas’ hearts are near the ventral
body wall and outside the area warmed by tunas’ vascular countercurrent heat
exchangers, the temperature of cardiac muscle will almost immediately reflect
changes in ambient temperature. This occurs regardless of body size or regional
endothermy (Sri11 et al., 1994).
12O 5
300
2
0 30
25
100
--+- muscle temperature
500 0
0100 0300 0500 0700 0900 1100 1300 1500 1700 1900 2100 2300
Fig. 11. Representative 24-h records (midnight to midnight) of the vertical movements of adult
yellowfin tuna (64 kg estimated body mass) and bigeye tuna (50 kg estimated body mass) in areas near
the main Hawaiian Islands. The former was carrying an ultrasonic depth-sensitive transmitter. and
swimming depth data were recorded approximately every IO s onboard a ship that was following the
fish. Temperature changes with depth were measured by lowering a temperature probe through the
water column and are plotted as 1°C isotherms. (Data replotted from Brill er al., 1999.) The bigeye
tuna was implanted with an archival (i.e., electronic data recording) tag that recorded swimming depth,
water temperature, and deep red muscle temperature every 8.5 min (R. Brill, M. Musyl, D. Curran.
and C. Boggs, unpublished observations). Note that the yellowfin tuna did not descend into water more
than =8”C below surface layer temperature (-25°C). In contrast, the adult bigeye tuna repeatedly
descended to water as cold as =7”C during the day (-0500-l 800 h) and thus repeatedly subjected its
heart to Q 18°C temperature changes.
As noted earlier, acute reductions in ambient temperature from 25 to 15°C

result in immediate and parallel decreases in heart rate and cardiac output (Q,”
of “2) in both yellowfin and skipjack tunas (Korsmeyer et al., 1997a; R. Brill,
K. Cousins, and T. Lowe, unpublished observations). Moreover, these do not ap-
pear to be neurally mediated effects, as the decline in heart rate with reductions in
ambient temperature is not counteracted by injection of atropine, a vagolytic drug

(St-ill, Cousins, and Lowe, unpublished observations). These studies imply, at low
ambient temperatures, that skipjack and yellowfin tunas have little or no ability to
increase cardiac output. Although they would be able to meet oxygen delivery
requirements at low swimming speeds, it seems unlikely that they would be able
to increase cardiac output enough to accommodate the doubling (or more) re-
quired during high-speed swimming, recovery from exhaustive exercise, and so
on. It is interesting to note that the apparent reduction in scope for activity results
from two of the facets that make tuna unique: a countercurrent heat exchange
system that will maintain metabolism of tissues at higher rates despite the colder
ambient temperature, and a heart that operates at maximal stroke volume. In oth-
ers words, since tuna hearts function on the upper (flat) end of their Starling
curves (Figure 5) and heart rate declines immediately with decreases in ambient
temperature, then maximal cardiac output declines in direct proportion to ambient
temperature. Unfortunately, thanks to the heat exchange system, metabolic de-
mand will not.
The next obvious question is how are bigeye tuna, and possibly other large
pelagic species such as bluefin tuna (‘Z’hunnus thynnus; Lutcavage et aZ., 2000;
Brill et al., 2000) and swordfish (Xiphias gkzdius; Carey, 1990), apparently able
to maintain cardiac function in the face of rapid ambient temperature change, and
thus achieve their extensive vertical mobility and apparent ability to exploit food
resources below the thermocline? There are several possible answers. Heart rates
may be less affected by temperature, or like other teleosts, they may be able com-
pensate for reductions in heart rate by increasing stroke volume. In the only in
vivo study of bigeye tuna physiology, fish exposed to hypoxia responded with a
bradycardia that was unaccompanied by increases in stroke volume, and cardiac
output fell with heart rate (Bushnell et al., 1990). It should be noted, however, that
both Freund (1999) and Shiels et al. (1999) found that acute temperature reduc-
tions increase Ca2+ release from the SR in isolated myocardial strips from yellow-
fin tuna. The Ca*+ sensitivity of isolated myofilaments from catfish (Pterygoplich-
thys spp.) is, however, temperature independent (Meadows et al., 1998). If the
same is true in tuna hearts, increased SR-Ca2+ release could step up cardiac con-
tractility in vivo and potentially offset the decrease in cardiac output resulting
from reduced heart rates. Isolated hearts from other teleosts (e.g., pickerel, Esox
niger) can maintain power output in spite of acute reductions in temperature from
15 to 5°C (Bailey et aZ., 1991). As stated, however, in vivo data suggest that any
temperature-induced increases in contractility occurring in yellowfin and skipjack
tunas are ineffective in maintaining cardiac output when these fish are subjected
to acute temperature changes. Clearly, the influence of environmental temperature
changes on cardiac function, both in vivo and in vitro, in a range of tuna species
is a subject that warrants further study.
VI. SUMMARY AND CONCLUSIONS
While significant gaps in our understanding of cardiovascular function in tu-

nas remain, available data, and the extrapolations constructed from them, are now
becoming consistent. For example, maximum measured heart rates, stroke vol-
umes, and reasonable arterial-venous oxygen content differences appear suffi-
cient to explain the (admittedly limited) data on maximum metabolic rates.
Several important anatomical adaptations allow tunas to achieve their excep-
tional rates of oxygen extraction from the ventilatory water stream and delivery
to the tissues. Tunas have gill surface areas approximately an order of magnitude
larger, and a blood-water barrier thickness up to an order of magnitude less, than
those of other teleosts. Tunas also have exceptionally large hearts. As a result,
even during periods of routine energy demand, high cardiac outputs are achieved
by large stroke volumes. To reach the cardiac outputs necessary to achieve their
exceptional maximum metabolic rates, tunas increase heart rate almost exclu-
sively, whereas other teleosts increase stroke volume almost exclusively or stroke
volume and heart rate about equally. The hearts of skipjack and yellowfin tunas
appear to rely more on sarcoplasmic CaZ+ release and resequestering during
routine functioning than the myocardium of other fishes, and probably on well-
developed specialized electrical conducting pathways as well.
For reasons that are not yet fully understood, tuna hearts normally function on
the flat upper limb of their Startling curve (i.e., they have a more limited ability to
increase stroke volume than do hearts of other teleosts). This characteristic may,
in turn, limit the vertical mobility of some tuna species (e.g., skipjack and yellow-
fin tunas). As water temperature decreases with depth, decreases in heart rate are
necessarily accompanied by decreases in cardiac output. Some tuna species (e.g.,
bigeye and bluefin tuna) appear to have evolved additional (e.g., Lowe et al.,
2000) but as yet mostly unidentified, physiological abilities that allow them to
expand their vertical range and thus exploit food resources in ways not available
to other tuna species. Due to the paucity of data gathered from members of the
family Scombridae, a careful comparative study on the physiological/biochemical
adaptations of hearts from various tuna and ectothermic scombrids will be fruitful
from both an evolutionary and a physiological perspective.
ACKNOWLEDGMENTS
The preparation of this manuscript was funded by National Marine Fisheries Service (Honolulu
Laboratory, Southwest Fisheries Science Center) and Cooperative Agreements NA37RJ0199 and
NA67RJ0154 from the National Oceanic and Atmospheric Administration with the Joint Institute for
Marine and Atmospheric Research, University of Hawaii. The opinions expressed herein are those of
the authors and do not necessarily reflect the views of NOAA or any of its subagencies. We gratefully
thank Barbara Block, Kathy Cousins, Laurent Dagorn, Heidi Dewar, Tony Farrell, Ellen Freund, David
Jones, Dave Marcinek, Holly Shiels, John Steffensen, and Yonat Swimmer for allowing us access to
unpublished data, reviewing drafts of this manuscript, and providing important ideas and insights. We
especially acknowledge Marvin Braun for his help with the section on the tuna bulbus arteriosus. Any
errors of omission or commission are, however, solely ours. This chapter is fondly dedicated to all the
colleagues we have had the pleasure and privilege of studying tunas with over the years-but espe-
cially to all those old friends who make us laugh.
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Wood, C. M., and Perry, S. F. (1985). Respiratory, circulatory, and metabolic adjustments to exer-
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Yamamoto, T. (1967). Observations on the fine structure of the cardiac muscle cells in goldfish. In
“Electrophysiology and Ultrastructure of the Heart” (Sano. T., Mizuhira, V., and Matsuda, R.,
Eds.), pp. l-13. Grune and Stratton, New York.
Yamamoto, K.-I., and Itazawa, Y. (1989). Erythrocyte supply from the spleen of exercised carp. Comp.
Biochem. Physiol. A 92, 139-144.
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4
ANATOMICAL AND PHYSIOLOGICAL

SPECIALIZATIONS FOR ENDOTHERMY
JEFFREY B. GRAHAM
KATHRYN A. DICKSON
I. Introduction
II. The Components of Tuna Endothermy
A. Sustained Swimming, a Continuous Source of Heat,
Allows Tunas to Maintain Elevated RM Temperatures
B. Metabolic Heat Conservation in RM
C. Maintenance of Elevated Temperatures in Other Tissues
111. A History of Discovery and the Development of Ideas about Tuna Endothermy
A. Early Observations
B. The Carey and Teal Era
C. Thermocentrism: Toward a Modern Synthesis of Tuna Endothermy
IV. Recent Laboratory Studies of Tuna Endothermy
A. Control of Heat Gain and Loss
B. Metabolic Performance
C. Tuna Locomotion, Endothermy, and Evolution
D. The Ontogeny of Tuna Endotherm)
E. Endothermy in Large Tunas
V. Effects of Endothermy on Some Cardiovascular Characteristics
A. Endothermy and Heart Function
B. Endothetmy and Hb-OZ Affinity
VI. Summary, Conclusions. and Future Directions for Laboratory Studies
I. INTRODUCTION
Tunas are endothermic, which means that they utilize metabolic heat to elevate
and maintain regional body temperatures (T,,) that are warmer than the ambient
seawater temperature (T,). The objective of this chapter is to review the contri-
butions made by laboratory investigations to our current understanding of endo-
thermy and its biological importance for these fishes. This will complement this
volume’s chapter by Gunn and Block, which reports on how information ob-
tamed from electronic tagging studies has contributed to our knowledge of tuna
endothermy.
121
122 JEFFREY B. GRAHAM AND KATHRYN A. DICKSON
For the purposes of this chapter “laboratory investigations” include dissec-

tion, measurement, and any other examination of fresh, frozen, or preserved tunas
for the purpose of understanding endothermy. Accordingly, we will discuss the
important perspective provided by comparative anatomical studies to current hy-
potheses about the origin and derivation of endothermy, as well as the ontogeny,
control, and biological significance of this specialization for tunas. “Laboratory
investigations” also include measurements of Tb, rates of temperature change, and
rates of heat production (mainly heat production by red muscle during swimming,
but also including that produced by the metabolism of different tissues) conducted
on live tunas.
The advantages of laboratory studies are that many of the important variables
such as swimming velocity, T,, and T,, are known and can be experimentally ma-
nipulated. Moreover, it is also possible to simultaneously monitor parameters di-
rectly relating to the endothermy mechanisms such as cardiac output and blood
0, levels, and to use animals in replicate experiments (Dewar and Graham, 1994;
Dewar et al., 1994; Korsmeyer et al., 1997a,b). By contrast, fewer variables can
be known for electronically tagged tunas swimming in the sea and, although future
developments in transmitter technology will increase the number of parameters
that can be monitored, there is not as much potential for controlled experimenta-
tion (Sri11 et al., 1994; Gunn and Block, this volume).
This does not, however, imply that laboratory studies lack disadvantages.
First, not all tuna species can be studied in a laboratory setting. Of the species that
can be so investigated, only small specimens can be used, and many factors related
to tuna endothermy are influenced by body size. Also, the physiological condition
of a laboratory tuna may be affected by diet, exercise regime, confinement within
the holding tank, or time in captivity. There is also a high level of stress associated
with “recapturing” and anesthetizing a captive tuna in order to affix the experi-
mental monitoring devices used in many studies. Because tunas are powerful and
struggle violently during capture, non-steady state conditions may exist for some
time after an experimental fish is handled. This and the tuna’s requirement for
constant swimming in near air-saturated water at the appropriate temperature
make laboratory experiments difficult and possibly of limited scope, unless the
fish can be stabilized and the experiment conducted for several hours or much
longer.
Capture stress and the requirements for swimming and respiration also limit
the success of efforts to return freshly caught, healthy tunas to a laboratory, al-
though this has been accomplished. At present three facilities in the western hemi-
sphere hold tunas for research purposes: the National Marine Fisheries Kewalo
Basin Tuna Facility in Honolulu, Hawaii, the Inter-American Tropical Tuna Com-
mission Laboratory at Achotines Bay, Panama, and the Stanford University and
Monterey Bay Aquarium Tuna Research and Conservation Center in Pacific
Grove, California. Studies relevant to tuna thermal biology have been conducted
at all three sites (Olson and Scholey, 1990; Brill, 1992; Dewar and Graham, 1994;
4. ANATOMICAL AND PHYSIOLOGICAL SPECIALIZATIONS FOR ENDOTHERMY 123
Dickson, 1994; Altringham and Block, 1997; Korsmeyer et al., 1997a,b; Farwell,
this volume). Tuna research cruises sponsored by the U.S. National Marine Fish-
eries Service (NMFS) Southwest Fisheries Center have also made important
contributions to the current understanding of tuna thermal biology (e.g., Laurs
et al., 1977).
This volume’s chapter by Collette, Reeb, and Block provides background in-
formation about tuna biology, nomenclature, and the evolutionary relationships of
tunas (tribe Thunnini) to the other fishes in the family Scombridae. The first ob-
jective of the present chapter is to provide a concise overview of the mechanisms
of tuna endothermy. This orientation to both the principles of heat transfer and the
special mechanisms for heat conservation found in tunas will set the stage for an
integrated assessment of the history of discovery and thinking about tuna endo-
thermy, primarily from the standpoint of the contributions made by laboratory
research. Then, we summarize what has been learned in more recent laboratory
studies of tuna endothermy, and suggest additional studies needed to lill gaps in
current knowledge.
II. THE COMPONENTS OF TUNA ENDOTHERMY
Among the tunas, elevation of myotomal muscle, eye, brain, and visceral tem-
peratures above water temperature has been documented. To maintain an elevated
temperature within any tissue, two conditions are necessary: (1) a source of meta-
bolic heat and (2) a mechanism to retain that heat. In most cases, the source of
heat for a tissue is its own intrinsic metabolic activity and, in all cases, the reten-
tion of this metabolic heat within the tissue requires the presence of arterial and
venous blood vessels arranged as countercurrent heat exchangers. Because all
tunas measured have been shown to conserve metabolic heat within the aerobic,
slow-twitch, myotomal muscle fibers (red muscle, RM) that power cruise swim-
ming, we will use information about the elevated T RMof tunas to illustrate heat-
transfer principles.
A. Sustained Swimming, a Continuous Source of Heat,

Allows Tunas to Maintain Elevated RM Temperatures
Tunas never stop swimming and thus continuously generate heat within the
RM. Steady and efficient cruise swimming and a capacity for powerful bursts are
fundamental features of tuna biology (Magnuson, 1973, 1978; Block et al., 1993;
Dewar and Graham, 1994). Selection for these attributes appears to have played a
role in this group’s evolutionary divergence from other scombrids about 40 million
years ago (Graham and Dickson, 2000). Constant swimming in tunas is, for ex-
ample, necessitated by the dependence upon ram gill ventilation (Roberts, 1978)
and by the requirement of a basal or minimum speed for generating hydrodynamic
lift (Magnuson, 1973, 1978). From an ecological standpoint, continuous swim-

ming in schools is important for tuna feeding success in the open ocean where
food resources are patchily distributed (Sund et al., 1981). Sustained cruising also
enables migrations to distant, high latitudes to take advantage of seasonally abun-
dant food resources and to make a timely return to warm waters for spawning.
Some tunas, for example, migrate across entire ocean basins twice a year (re-
viewed by Joseph et al., 1988). Tunas also make rapid vertical migrations in
search of prey and, in so doing, must be able to adjust to or compensate for
changes in light, oxygen, temperature, and hydrostatic pressure-all of which can
potentially affect the sensory and motor functions necessary for prey capture.
Because it functions aerobically, RM sustains the power requirements of con-
tinuous swimming. Although tuna dependence upon RM for this function is simi-
lar to that of other cruise-adapted species, tuna RM has unique properties. When
its in vivo temperature is taken into account, tuna RM has higher aerobic enzyme
activities (and these are matched by higher myoglobin concentrations) relative to
the RM of other active fishes, including the ectothermic scombrids (Dickson,
1996). Tuna RM is located in a different position within the body than it is in all
other teleosts, (with the exception of the swordfish Xiphias gludius, Figure 1). In
Fig. 1. Transverse sections showing differences in the position of the slow-twitch, oxidative my-
otomal muscle (RM) between an ectothermic scombrid (Sardu chiliemis, A) and a tuna (Allothunnus
fallui, B). The RM fibers (outlined in white on the right of each section) form a lateral wedge adjacent
to the skin in ectothermic scombrids, with some RM penetrating along the horizontal septum to the
vertebrae in Sarda, and are in a more medial position in the tunas.
0 ectothermicscombrids
- O.9-
l tunas
! 0.8 -’
I 0.7 -
6
q 0.8 -
e
8 0.5 -
unnus albacares
Scomberjaponicus
i::-
Uoihmnus falai
Sad3 orbnialis
nosarda unicolor
0 2 4 8 8 10 12 14
Rebthfe Red Muecie Mass (% of body maas)
Fig. 2. Relationship between relative heart mass and relative red muscle mass in 10 scombrid
species: Relative Heart Mass (%) = O.O59[Relative Red Muscle Mass (%)I + 0.018, rz = 0.95. Error
bars represent 95% confidence intervals of mean values for species when n 2 3. Data are from Graham
et al. (1983) and Graham and Dickson (2000): graph is from Graham and Dickson (2000).
all other cruise-adapted bony fishes, including the ectothermic scombrids, RM

occurs along the horizontal midline near the lateral edge of the body, just beneath
the skin. Tuna RM is both more anterior and nearer to the vertebral column and is
completely surrounded by white muscle (WM; Kishinouye, 1923; Graham et al.,
1983). This RM position and its specialized connective-tissue linkage to the cau-
da1 fin affects swimming mechanics and results in the unique tuna swimming
mode which is termed “thunniform locomotion.” Features of the thunniform lo-
comotion pattern include minimal lateral body flexion and changes in the relation-
ships between muscle activation and the strain cycle (Graham et al., 1983; West-
neat et al., 1993; Block and Finnerty. 1994; Shadwick et al., 1999; Ellerby et al.,
2000). The relative amount of RM varies among tuna species. In Auxis thuzurd
and Euthynnus lineutus, for example, RM composes more than 10% of total body
mass. However, in other tuna species, relative RM amounts range from 4.1 to 8.4%
of total mass, which is similar to amounts in ectothermic scombrids (reviewed by
Dickson, 1995). Another difference in tuna RM is a lower scaling coefficient for
RM mass with respect to body mass than is found in the ectothermic scombrids
Surdu chiliensis and Scomher japonicus (Graham et ~rl., 1983). Among the scom-
brids that have been examined, a significant positive relationship exists between
mean relative RM mass and mean relative heart mass (Figure 2). This is expected
because of the role of RM in powering sustained swimming and that of the heart
in providing 0, and metabolic fuels to RM. This relationship also suggests that,
in view of the allometric scaling of RM mass in tunas, the relative size of the tuna
heart may also decrease with body size, as has been found for some tuna species
(Graham et al., 1983).
B. Metabolic Heat Conservation in RM
1. RETIA MIRABILIA
Oxidative heat production by continuously active RM occurs in all fishes.
What distinguishes tunas is that circulation to and from the RM is by way of
countercurrent heat exchangers, termed retia mirubiliu (wonderful nets), which
conserve heat and establish a stable thermal gradient or thermal excess (T, =
T, - T,). The RM retiu mirubiliu are vascular bundles composed of sheets
of parallel arterial and venous blood vessels that are intimately juxtaposed (Fig-
ure 3). To distinguish heat-exchanging retiu from other countercurrent exchange
vasculatures such as those associated with teleost gas bladders, previous workers
emphasized that heat-exchanging retiu were composed of small arterial and ve-
nous vessels rather than capillaries (Carey and Teal, 1966; Stevens et al., 1974;
Txab-,
Gills Red muscle
L,V a a
Heart
-.
. , ,, 0
u I
TxvbJ Txm
Fig. 3. Schematic showing the position of the central r&al heat exchanger on the major systemic
blood supply (the dorsal aorta and postcardinal vein) of the skipjack, Katsuwonus pelamis. Arrows
indicate flow direction: arterial inflow is from the gills and venous outflow is to the heart. The three
TX positions illustrate thermistor positions for determination of temperatures in the RM (m), the ventral
aorta (vb), and the dorsal aorta (ab) during the heat-pulse experiments of Stevens and Neil1 (1978; also
see Figure 5). (From Brill er al., 1994.)
Graham and Diener, 1978). New structural evidence shows that these vessels are,
in fact, arterioles and venules; the diameters of the vessels fall within the ranges
for vertebrate arterioles and venules, and the vessel wall ultrastructure resembles
these types of vessels (Moore, 1998). Venules exiting the RM carry heat generated
by aerobic metabolism and, as this venous blood passes in close proximity to the
oppositely flowing cool arterial blood, thermal equilibration occurs. Because ther-
mal diffusion occurs rapidly and the vessel walls are several cell layers thick, only
heat is transferred within the retia. The RM retiu of tunas contain more arterioles
than venules (Table I) but, because the venules are larger, they compose a greater
volume of the structure (Graham and Diener, 1978; Graham, 1983).
In the four species that have been examined (Euthynnus lineatus, Katsuwonus
pelamis, Thunnus albacares, and Thunnus alalunga), the rete arterial vessel walls
contain two or three layers of smooth muscle while the venule walls have a single
layer (Figure 4). Varying the contractile state of the vascular smooth muscle pro-
vides a possible mechanism whereby vessel diameter and thus blood-flow and
heat-exchange effectiveness may be adjusted in vivo. Although rete blood-flow
characteristics have not been examined, preliminary data from restrained kawak-
awa (Euthynnus a&is) suggest that the intravenous administration of catechol-
amines affects retial heat-exchange efficiency (Brill et al., 1994), which may be
mediated by alterations in rete vessel diameter.
2. RETIADISRUPT THE BALANCE BETWEEN HEAT

PRODUCTION AND HEAT Loss IN RM
As originally emphasized by Carey and Teal (1966), the importance of heat-
conserving retiu to tuna endotbermy cannot be overstated. Fish lacking retia can-
not block the convective transfer of heat to the gills. Because the heat capacity of
water (1 cal g-’ “C-r) is four times greater than that of air and because thermal
diffusion occurs about 10 times faster than molecular diffusion, blood residing in
the gills for the time required for respiratory gas exchange would also reach ther-
mal equilibrium with the water (Graham, 1983).
The critical need for RM heat conservation is illustrated by the relationship
between its heat production (HP,& and the potential branchial heat loss rate
W- G,LLS)in a steadily swimming fish that lacks heat-conserving retia. Heat pro-
duction depends upon 0, delivered by the blood to the aerobically powered RM
fibers,
HP,, = Q dKh1, v . 0, Cal, (1)
where Q (ml min-I) is the blood-flow rate to RM, d[O,],-, is the quantity of O2
consumed by RM [i.e., arterial - venous 0, content (ml 0, min-I)], and 0, cal is
the oxycalorific equivalent [the quantity of heat produced per unit of 0, consumed
(cal ml-’ O,)]. [Note that the units for HP aMin Equation (1) are cal time--‘.]
Blood also has a high heat capacity, which means that heat formed in the RM
Table I
Summary of Published Data on Some Characteristics of the Arterial (A) and Venous (V) Blood Vessels of Tunas’
Central R&a, Countercurrent Heat Exchangers Serving the Red Myotomal Muscle
Fish fork Mean ratio Inside diameter Inside diameter

Species length (cm) A:V arteriole (pm) 0 venule ( ym)” Reference
Euthynnus linratus 49.2 1.04 53.9 ? 4.6 (20) 109.5 2 6.2 (20) Graham & Diener, 1978
12.9 1.11 No data No data Dickson, 1994
Kutsuwonus pelamis 42.1 1.11 35.7 t 1.3 (706) 83.8 k 4.5 (637) Stevens et al., 1974
49.7 No data 36.6 + 7.9 (10) 79.0 c 3.9 (1 I) Graham & Diener, 1978
Thunnus albacares 55.5 1.48 33.5 t 2.2 71 .O i 3.6 Koehm, 1980
66.5 I .44 43.5 5 2.0 115.9 t- 2.2 Koehm, 1980
“Values are +SD (number of vessels measured).

Fig. 4. Transverse sections of (A) a lateral rere arteriole from the skipjack tuna Kursuwonus
pelamis, (B) a portion of the wall of a refe arteriole from albacore, 7humus alalunga, and (C) a central
rete venule from K. pemmis. The scale bar represents 10 pm in A and C and 2.5 pm in B. E, endothe-
ha1 cells; EI, elastica intema; L, vessel lumen; rbc, red blood cell; S, smooth muscle cell; and W
indicates the wall thickness of the venule. All images are from 1-pm-thick sections cut on an ultra-
microtome from plastic-embedded, glutaraldehyde-fixed rete specimens, and viewed at low power on
a Hitachi H7000 transmission electron microscope. (Photo montages prepared by S. Karl and
J. Moore.)
130 JEF'FREYB.GRAHAMANDKATHRYNA.DICKSON
has a high probability of diffusing into the capillary blood and being transported
to the gills. In fact, the heat capacity of blood plasma meets or exceeds the quantity
of heat that can be formed from the quantity of 0, transported. Thus, I&o,, (cal
time-l) is also described in terms of blood flow,
HL GILLS= Q . St,,,, . Tx m,, (2)
where Q is RM blood-flow rate (ml mu-‘), Sb,oadis blood heat capacity (cal ml-’
‘C-l), and TXRMis the rise in blood temperature caused by the release of RM heat
produced from the 0, consumption. Equations (1) and (2) show that the rate of
blood flow through RM governs both heat production and heat loss. If flow in-
creases, more Oz is provided for heat production but there is also more convective
heat loss. Thus,
and TM does not change.

Discussion to this point has considered HPRhl in the absence of any heat-
conserving capacity. Also, RM has been the focus of the discussion. However, the
principles that have been developed apply to any aerobic tissue (i.e., which is
generating metabolic heat in conformance with the first law of thermodynamics)
and, as will be discussed below, other tissues within tunas generate sufficient heat
to raise regional temperature. The important message at this point is that, irrespec-
tive of where the tissue heat source is placed, it is a physical impossibility for an
active fish lacking a vascular heat exchanger to maintain a T,, that is more than
1°C warmer than T, under steady state conditions (i.e., when heat production =
heat loss; Brill et al., 1994). It is the retention of RM heat by the retie that enables
tunas to be endothermic, and several studies of reti& heat-exchange efficiency
have been done.
3. RETIAL EXCHANGEEFFICIENCY:THEKEYTOTUNA
END~THERMY
Retial efficiency in heat exchange was first estimated by Stevens and Neil1
(1978), who applied a heat pulse to the water perfusing the gills of a restrained
(ventilated and slightly anesthetized) skipjack tuna (Kutsuwonus pelumis, Fig-
ure 5). Thermistors monitored temperatures in the gills, ventral aorta, brain, RM,
and venous blood, and heart rate (HR) was also recorded. A square-wave heat
pulse was applied by switching to 5°C warmer perfusion water for 15 s. Figure 5
shows the immediate rise in gill temperature as well as the appearance of the heat
pulse in the ventral aorta within lo-15 s after it was given. This is about three
times faster than if the pulse had transited the entire circulation. Because the
heated aortic blood traversed various routes through the systemic circulation,
warmed blood continued to return to the ventral aorta for about 2 min.
The heart of all tunas operates at or very near to T, (Graham, 1983) even in
i?! 4.0 - RED MUSCLE EXCESS

2 g 3.0 -
f%
(n%G e 2.0 -
F 1.0 - BRAIN EXCESS
VENo”s BL00D 4 14 COI. out

EXCESS
2a- 157 col. in
n
al 27-
&5
26-
p!! !~ SKIPJACK TUNA 1.3 kg
EE a- 25-
“e 24”
GILL WATER
23- :
c
$m
z 0.5- HR 163 HR 175
mm
,5 If 0.3- -~ ~.
--,ra
52 ID- O.l-
E
I~~~~~~~~~~~~~~..“.““~~~.~~~“~
TIME (5 set)
Fig. 5. Effects of a heat-pulse application to the ventilatory stream of a restrained skipjack tuna.
See text for details. Refer to Figure 3 for the genera1 circulation scheme and to see placement sites of
the venous blood and RM muscle thermistors. Note that neither the RM nor the brain registered in-
creases in T,, but that a rise in venous blood TX occurred shortly after pulse delivery. (From Stevens
and Neill, 1978.)
fish with a high T, (Carey et ul., 197 1). The skipjack’s initial heart rate of 163 bpm
increased to 175 bpm late in the heat-puise delivery, indicating that some warming
of the heart had occurred, probably as a result of thermal conduction (defined as
the diffusion of heat from molecule to molecule down the thermal gradient in a
solid object) from the branchial to the pericardial cavity, and the return of warmed
venous blood to the heart (Stevens and Neill, 1978). However, Figure 5 shows that
the heat pulse did not arrive at the RM or the brain because it was transferred from
the arterial to venous circulation by the skipjack’s heat exchangers.
By assuming that gill blood came into complete thermal equilibrium with the
heat pulse, Stevens and Neil1 (I 978) estimated the quantity of heat added to dorsal
aortic blood to be about 150 cal and the amount of heat returning in the venous
circulation to be about 110 cal. Thus, the skipjack retial system was at least 75%
efficient.
While this level of efficiency seems impressive, the estimate of Stevens and
Neil1 may be low for several reasons (reviewed in Brill et aZ., 1994). These work-
ers did not know the percentage of cardiac output going to the RM (and thus
reflected by the central rete) but reasoned that, because over 50% of the heat return
occurred within 40 s, about 50% of the cardiac output went into the retia serving
RM. Using radioactive microspheres and working at sea aboard the R/V David
Starr Jordan, White and co-workers (1988) determined that about 36% of the
cardiac output flowed to the RM of the albacore (7’hunnus alulunga). Because the
albacore has a smaller RM mass than the skipjack (4.1 vs. 7.5%; Magnuson, 1973;
Graham et al., 1983), the proportionally larger Stevens and Neil1 estimate of 50%
of cardiac output to RM in skipjack seems reasonable.
With additional data such as cardiac output to RM, better estimates of retial
exchange efficiency became possible (Graham, 1983; Brill et al., 1994). These
reveal the interdependence of 0, delivery, heat production rate, and blood flow in
determining the level of retial exchange efficiency needed to sustain a specified
T,. Figure 6 illustrates this for a lo-kg albacore, with 410 g of RM that receives
about 36% (White et al., 1988) of the cardiac output (which is 108 ml mini).
Because each milliliter of arterial blood contains nearly 0.2 ml O2 (Stevens and
Neill, 1978), oxygen delivery is about 0.053 ml O2 min-’ g-l [i.e., 108(0.2)/410].
Assuming a RM metabolism of 0.124 cal min-’ g-l (Stevens and Neill, 1978) and
an oxycalorific equivalent of 4.7 cal ml-’ 02, 0.026 ml 0, min-’ g-’ is required at
low swimming speeds, which is about 50% of the 0, quantity being delivered. If
total RM heat production is 50.8 cal mm’ (0.124 X 410), a metabolic heat incre-
ment of 0.47 cal ml-’ will be applied to capillary blood (50.8 cal minV108 ml
min-I). Assuming 50% of this heat is conducted into the surrounding WM (Fig-
ure 1) and a T, of 10°C a 97% efficiency is needed to maintain a stable T,
(Figure 6A). Figure 6 also shows how efficiency requirements change with T, and
with 0, utilization. If 85% of the available 0, is consumed (Figure 6B), RM heat
production rises to 8 1.2 cal min- ’ and the thermal increment increases (8 1.2/108
= 0.75 cal ml--‘); however, and allowing for 50% conductance to the WM, a retial
efficiency of 96.3% is still required to maintain a 10°C T,. Even if blood-flow rate
and RM 0, consumption were dramatically elevated (Figure 6C), a 96% efficiency
is required to maintain a 10°C T,. Thus, 0, delivery and RM heat production are
tightly linked to blood flow, which has the potential to carry heat away as fast as
it is produced. High retial exchange efficiencies are required to prevent this (Fig-
ure 6D); the minimum efficiency needed to defend a steady state T, of 2°C is about
75%, the level measured by Stevens and Neil1 (1978).
4. INTERSPECIFIC DIFFERENCES IN THE

STRUCTURE OF RM RETIA
Retia occur adjacent to the RM in all tuna species, but there are interspecific
differences in rete size, complexity, and position (Graham, 1975; Stevens and
Neill, 1978; Bushnell et al., 1992). Many tunas have a central rete [Auk spp.,
4. ANATOMICAL AND PHYSIOLOGICAL SPE(‘1.4LI~.4TIONS I-OK ENDOlXI:K~l? 1.a.;
Blood flow 108 ml min-1

Conduction 0.235
TX 80-
0.38
60-
““V TX
15
Fig. 6. Effects of RM 0, utilization (heat production) on the level of retial heat-conservation

efficiency required to maintain a constant temperature in the RM. The model is for a lo-kg albacore
having 410 g of RM that receives 36% of cardiac output, or 108 ml min-‘. Comparison of A and B
shows that to conserve TX, a rise in the consumption rate from 50 to 85% of the O2 arriving in the RM
must be accompanied by a slight drop in exchange efficiency (assuming no change in blood flow). C
shows that a IO-fold increase in Oz uptake, when accompanied by a sixfold increase in blood flow,
does not alter the requisite efficiency. D illustrates how, under conditions in A, r&d exchange effi-
ciency is affected by T,. (From Graham in Fish Biomechanics, P. W. Webb and D. Weihs, Eds. Copy-
right 0 1983 by Praeger Publishers. Reproduced with permission of Greenwood Publishing Group,
Inc., Westport, CT.)
Euthynnus spp., Katsuwonus pelamis, Thunnus tonggol, Thunnus atlanticus, and
Thunnus albacares (Graham, 1975; reviewed by Bushnell et al., 1992), and Allo-
thunnus fallai (Graham and Dickson, 2000)] supplied by the dorsal aorta and post-
cardinal vein. All tunas except A. fallai (Graham and Dickson, 2000) have lateral
retia, which are supplied via the lateral arteries and veins. Among teleosts, these
lateral blood vessels (which have also been termed cutaneous or subcutaneous
vessels) are found only in the tunas.
C. Maintenance of Elevated Temperatures in Other Tissues
Some tunas have the capacity to warm other body regions and, in all such
cases, retia positioned at critical sites are required to conserve this heat and main-
tain elevated temperatures (Linthicum and Carey, 1972; Bushnell et al., 1992).
Euthynnus spp., Katsuwonus pelamis, and Thunnus spp. have warm brains and
possess retiu on each carotid artery to warm blood entering the brain. The heat
source for brain warming in tunas is unknown. It may arrive by thermal conduc-
tion through myotomal muscle via the frontoparietal fenestrae that are found in
the skulls of all tuna species that can maintain elevated brain temperatures (Gra-
ham and Dickson, 2000), or metabolism within the central nervous system or the
extraocular muscles may be the heat source (Linthicum and Carey, 1972).
Retia also conserve heat in the viscera of several Thunnus species (T. albaca-
res, Z obesus, T. maccoyii, T. alalunga, and lY thynnus; see Table 11). Facultative
heating of the stomach occurs after feeding in the bluefin, T. thynnus (Carey et al.,
1984). Digestion, absorption, and anabolic processes within the stomach and par-
ticularly the caecal mass, the warmest visceral organ in T. thynnus, are most likely
the primary source of heat for visceral warming in tunas (Carey et al., 1984).
The rates of heat production by these tissues are not as well quantified as the
rates for RM. Visceral heating, for example, occurs only after feeding and may
therefore be largely intermittent. Nevertheless, and regardless of the rate and site
of heat production, it is important to emphasize that, if cool arterial blood destined
for either the warm brain or warm visceral cavity was not warmed (by venous
blood draining these tissues) prior to entering these regions, an elevated regional
temperature could not be maintained (Carey et al., 197 1; Graham, 1983).
III. A HISTORY OF DISCOVERY AND

THE DEVELOPMENT OF IDEAS
ABOUT TUNA ENDOTHERMY
The first principles for heat conservation provide the basis for reviewing the
history of laboratory studies of tuna endothermy. Historical accounts of discov-
eries related to tuna T,, are contained in Stevens (197Q Stevens and Neil1 (1978),
Dizon and Brill (1979a,b), Graham (1983), Brill et al. (1994), and Fudge and
Stevens (1996). The purpose of this section is to integrate the chronology of pri-
marily laboratory discoveries about endothermy with the evolution of the diverse
ideas suggested about the advantages, limitations, biological significance, and
evolutionary origins of endothermy.
A. Early Observations
British physician John Davy (1835) was the first to document the warmth of
tunas. He observed that skipjack (Katsuwonuspelamis) in waters near Ceylon had
a “temperature of 99°F when the surrounding medium was 80”F, and it consti-
tuted an exception to the generally received rule that fishes are universally cold
Table II
Probable Importance for Endothermy Proposed by Graham (1975) of Some of the Taxonomic Characters
Used by Gibbs and Collette (1967) to Distinguish the Species of the Genus Thunnus
Probable importance
for endothermy Character T alalunga 7: thynnus Z maccoyii 7: obesus T albacares T: atlanticus T. tonggol
Index of body shape and the extent Cutaneous artery branch- 3-4 3-4 3-4 6-8 6-8 6-8 6-8
of anterior-lateral RM position point from the dorsal
aorta (vertebra number)
Index of relative lateral r&d sur- Number of arteriole rows I 2 2 2 1 I 1
face area branching from the cu-
taneous artery
Presence/absence of postcardinal Postcardinal vein I’ Absent Absent Ahsent Present ” Present Present Pre4ent
vem indicates whether or not
there is complete central
circulation
Position of articulating surface in- Position of the haemal pre- On Near Near Near Well Well Well
dicates quantity of haemal arch zygapophyses on ante- centrum centrum centrum centrum ventrad ventrad ventrad
open space for central rior vertebrae
circulation
Another indication of greater hae- Length of the haemal Short Short Short Short Long Long Long
ma1 arch open space postzygapophyses on
the anterior vertebrae
Indicates a large lateral aperture Ventroiateral foramina size Small Small Small Small Large Large
for rete vessels supplying RM
Indicates capacity for facultative Liver striations and vascu- Present Present Present Present Absent Absent
heating of viscera lar retia
“Incomplete central circulation necessitates greater reliance upon lateral circulation for RM and WM perfusion.
“7: obeus has a postcardinal vein but not a central rete.
’ ‘f. albacares has a caecal rete(Block, personal communication).
blooded.” [An annotated copy of Davy (1835) and another of his papers on tuna
temperature (Davy, 1844) are contained in Fudge and Stevens (1996).]
At the time of Davy’s work, the role of the respiratory organs and blood, in
particular the erythrocytes, in supplying 0, to the body was not understood. The
concept of metabolic heat did not exist and it was thought that, while some ani-
mals (endotherms) produced heat, cold-blooded animals (ectotherms) did not.
Linnaeus, for example, had distinguished animals on the basis of temperature and
used the phrase “sanguine frigido” to describe ectotherms. The generality of fish
“cold bloodedness” had been proclaimed by Georges Cuvier in the Historie Na-
turelle des Poissons: “Ne respirant que par l’intermede de l’eau, c’est-a-dire, ne
profitant pour rendre a leur sang les qualite d’oxigene contenu dam l’air mele a
l’eau, leur sang a dfl rester froid” (Cuvier and Valenciennes, 1828, 275). Volume
VIII of that same work (Cuvier and Valenciennes, 183 1,64 - 65) detailed features
of the specialized lateral circulatory anatomy of tunas. Cuvier and Valenciennes
did not interpret the function of this structure, nor did their descriptions of the
tuna viscera indicate that they had observed the visceral retia. Eschricht and
Mi.iller (1835) made the first descriptions of the visceral retia of the bluefin tuna
and, knowing of Davy’s findings, they made the link between the arrangement of
arteries and veins in the “Wundernetze” (retia mirabilia) of this organ with the
warmth of tunas. However, they did not articulate the principle of countercurrent
exchange, and neither the source nor the mechanism of heat generation was
known.
The link between tuna vascular anatomy, activity level, and an elevated body
temperature was suggested by Kamakichi Kishinouye, who in 1923 published a
remarkable treatise on the autecology of tunas and other scombrids, “Contribu-
tions to the Comparative Study of the So-called Scombroid Fishes.” This work,
the single most comprehensive treatment of scombrid biology ever written, fo-
cused mainly on species in Japanese waters. Kishinouye provided information
about most aspects of tuna and scombrid biology, including feeding, development
and growth, distribution, locomotion, migration, predators, and parasites. He also
compared their skeletal, muscular, nervous, sensory, digestive, renal, reproductive,
respiratory, and vascular systems. An especially valuable feature of Kishinouye’s
monograph was that it was published in English. Another was that it contained
large color plates and line drawings of tuna vascular anatomy that were accom-
panied by written descriptions of other structural details. The illustrations have
appeared in several volumes on tunas (Sharp and Dizon, 1978; Fudge and Stevens,
1996) and the Traite de Zoologie (Bertin, 1958). Kishinouye also provided nu-
merous comparative details about RM (chiai) structure in different scombrids,
illustrated its different positions in tunas and bonitos (Sarda), and showed the
intimate relationship between RM and the special vascular complex adjacent to it
[kurochiai (= retia)] in tunas.
Based on the unique circulatory features of tunas, especially the prominent
lateral vessels, Kishinouye (1923) proposed placing the tunas in their own order,
4. ANATOMICAL AND PHYSIOLOGICAL SPECIALli’sATlONS FOR ENDOTHERMY 137
the Plecostei, to distinguish them from all of the other modern teleost fishes. Al-
though this proposal for a major revision of fish systematics was not adopted,
Kishinouye’s monograph was unprecedented at the time for its synthesis of tuna
biology. As modem interest in the anatomical and physiological bases of tuna
endothermy developed in the mid-1960s comparative physiologists and anato-
mists rediscovered this work and, some 7.5 years after its publication, Kishinouye
(I 923) remains a fundamental contribution.
B. The Carey and Teal Era
The mid-1960s saw the beginnings of the explosive growth in the rate of dis-
covery and insight in most areas of science, and the biology of tunas was no ex-
ception. Very little tuna T, data were obtained in the interval from Davy’s first
report to the early 1900s [reviewed by Carey and Teal (1966) and Stevens (197X)].
Barrett and Hester (1964), who used electronic thermometers, began the modern
era of tuna T, measurements. Working with freshly caught skipjack (Kutsuwonu.r
pelamis) and yellowfin (7’hunnu.r albacares), these workers demonstrated one
physiological feature of tuna endothermy, the tendency for the TX (= T, - T,,) to
be lower for fish caught in warmer waters, particularly in the skipjack.
However, it was the publication of “Heat Conservation in Tuna Fish Muscle”
by Francis Carey and John Teal (1966) that ignited this field. This paper pre-
sented new T, data, provided the Hurstillustrations of thermal profiles, and detailed
the anatomical and physiological bases for tuna thermoconservation, including
the direct dependence of metabolic heat production on the delivery of oxygen.
Further, this work also elucidated the biophysical and biochemical principles un-
derlying the physical challenges for, and biological advantages afforded to, a
warm fish.
Over the next 25 years. Carey and co-workers added many details about fish
endothermy, including documentation of elevated brain, eye, and stomach tem-
peratures in certain tunas (Carey et al., 197 1; Linthicum and Carey, 1972; Stevens
and Carey, 1981); evidence of the bluefin tuna’s capacity to thermoregulate (Carey
and Teal, 1969a; Carey and Lawson, 1973): demonstration of endothermy and
elevated visceral temperatures in the lamnid sharks (Carey and Teal, 1969b; Carey
et al., 1981; Block and Carey, 1985); and description of the structural and bio-
chemical modifications in swordfish eye muscles that permit elevated brain and
eye temperatures (Carey, 1982; Block, 1986). These works more than any others
have set the pace for this field and, while the scope of the fish endothermy problem
has evolved considerably since Carey and Teal (1966), this work remains a fre-
quently cited reference and is noteworthy because of its breadth of coverage and
concise elucidation of first principles.
While Carey and Teal’s 1966 paper established the field of tuna thermal biol-
ogy, it made little reference to the evolution of tunas or to how interspecific dif-
ferences in body form or circulation might affect swimming performance or
heat conservation capacity. Two other important papers on tuna biology that
appeared about the same time as Carey and Teal (1966) were “Comparative
Anatomy and Systematics of the Tunas, Genus Thunnus” (Gibbs and Collette,
1967), and “Studies in Locomotion and Anatomy of Scombroid Fishes” (Fier-
stine and Walters, 1968). Most tuna biologists would agree that these papers,
along with Carey and Teal (1966), form the foundation of our current understand-
ing of tuna endothermy.
However, as important as these papers were, they did not make reference to
one another. When these works appeared there was not a large critical mass of
tuna biologists, and most of the work being done focused on fisheries questions.
A unified understanding of the systematics, distribution, and movements of these
widely distributed, commercially important species was a critical issue for stock
assessment and management. The treatise on the taxonomy and biology of the
seven species of Thunnus by Gibbs and Collette (1967) clarified and standardized
what had been an arcane and provincial nomenclature. It also compared the mor-
phologies, natural histories, and depth distributions of the Thunnus species and
detailed many of the comparative differences in the skeletal and vascular systems
that were used by Gibbs and Collette to distinguish between members of the genus
(Table II). While Gibbs and Collette did not specifically discuss what role “heat
conservation” might have played in the evolution, radiation, and geographical dis-
tribution of Thunnus species, the vascular and vertebral skeletal differences they
noted for the two subgenera are now regarded as indicators of endothermic capac-
ity that correlate with the penetration of T. alalunga, T. maccoyii, T thynnus, and
7: obesus into deeper and cooler waters (Graham, 1975). Thus, what was impor-
tant for the comparative physiologists and anatomists interested in tuna endo-
thermy was that, in addition to providing important morphological information,
the paper by Gibbs and Collette (1967), several other works by Collette and co-
workers (Collette and Chao, 1975; Collette, 1978, Collette et al., 1984), and some
earlier studies (Godsil and Byers, 1944; Godsil, 1954) established an authoritative
reference point for defining and understanding the relationships among the now
five genera and 15 species of tunas and for comparing the tunas (tribe Thunnini)
to their sister group, the bonitos (tribe Sardini; Graham and Dickson, 2000; Col-
lette, Reeb, and Block, this volume).
Fierstine and Walters (1968) examined skeletal and morphological differences
in bonitos and tunas that relate to the tuna’s stiffer (tbunniform) swimming mode,
and in so doing provided the first information on scombrid swimming biomechan-
its. These workers described the deeply nested myotomal cones of scombrids and
contrasted the myotomal structures of the tunas and bonitos, which differ in cone
thickness and length as well as in the relative amount and position of RM. How-
ever, Fierstine and Walters (1968) did not consider the implications of the tuna’s
elevated TRMfor its swimming performance relative to the bonito.
Magnuson (1973) examined scombrid locomotion and compared functional
differences in tunas and other scombrids. Working with live fish at the Kewalo
Basin Facility in Hawaii, he measured the swimming velocity of different scom-
brids and developed a hydrodynamic model predicting the basal swimming ve-
locity (i.e., the minimum speed for hydrodynamic equilibrium) of a species based
on morphological characteristics such as body shape, thickness, density, mass-
length ratio, and area of the pectoral fin (and other lifting surfaces). Magnuson
also found a correlation between basal speed and the relative amount of RM and
blood hemoglobin (Hb) concentration, concluding that scombrid aerobic capacity
had been directly influenced by requirements for sustained swimming. Magnuson
did not consider the question of tuna endothermy, but his data indicated that, for
tunas (Ku~~uwonus, Euthynnus) and ectothermic scombrids (Surda) having about
the same basal speeds, the tunas had both more RM and more Hb. This was quite
intriguing to physiologists interested in endothermy because it suggested that tuna
RM quantity was more than adequate to power basal swimming speed, and that
tunas incurred a greater metabolic cost because they had more and warmer RM
(Graham, 1975; Sharp and Pirages, 1978).
Thus, when the works of Carey and Teal, Gibbs and Collette, and Fierstine
and Walters appeared, it was not expected that answers to questions that have
occupied tuna physiologists for the past 30 years (viz., Why and how did endo-
thermy evolve? How is it regulated? What is its functional significance? Why is it
present in tunas but not other scombrids?) would be answered in part by the inte-
gration of information contained in these three seemingly disparate works. Com-
parative biologists who became interested in tuna endothermy at that time were
inspired by the discoveries of Carey and his colleagues, could be confident of the
foundations in tuna morphology and systematics provided by Gibbs and Collette
and others, and, thanks to the contributions of Fierstine and Walters and Magnu-
son, could begin to see the outlines of the relationship between tuna vascular spe-
cializations, swimming activity, and an elevated T,, that had been suggested by
Kishinouye. As the remainder of this chapter will show, interrelationships among
mechanisms affecting heat gain and loss (principally swimming velocity and T,),
the physiological effects of elevated temperature on the physiology (including
swimming performance), ecology, and evolutionary radiation of tunas, and the
influences of large-scale changes in ocean ecology and thermal structure occur-
ring over geologic time all appear to have had a major influence on the evolution
of tuna swimming performance and endothermy, which in turn influenced this
group’s adaptive radiation (Graham and Dickson, 2000).
C. Thermocentrism: Toward a Modern Synthesis

of Tuna Endothermy
The conclusion of the 1978 review of tuna thermal relations by Stevens and
Neil1 was titled “A Thermocentric Overview of Tuna Evolution.” That title was
appropriate then and it remains so now. Most investigators would agree that tuna
thermal relations are as fundamental to their biology as is swimming. In the next
section we describe four categories of laboratory research on tuna endothermy:
(1) the capacity of tunas to regulate heat gain and loss, (2) the effects of tempera-
ture on tuna metabolic processes, (3) the combined effects of tuna endothermy
and enhanced swimming performance on this group’s evolutionary radiation, and
(4) the ontogeny of tuna endothermy.
However, before ending this discussion of the history of research into and
ideas about tuna endothermy, it is important to consider some of the factors that
influenced the direction of the laboratory work. Fisheries issues such as the east-
ern tropical Pacific tuna-porpoise problem increased the need to develop more
precise models for predicting (for commercial purposes) tuna movements, and
these began to use physiological data to better define the role that ambient tem-
perature and dissolved oxygen might play. For example, the model of Barkley
et al. (1978) suggested that, for larger Kutsuwonus, the intersection of limiting
thermal and oxygen isopleths made large regions of the eastern tropical Pacific
uninhabitable (Sri11 and Bushnell, 1991; Korsmeyer et al., 1996a,b). To refine
such predictions, experiments at Kewalo Basin tested the ability of tunas to per-
ceive temperature gradients and determined the effects of different 0, levels and
T,‘s on swimming velocities (Stevens and Neill, 1978; Dizon et al., 1978; Brill,
1992). A related idea was that tunas were prisoners of their efficient thermocon-
serving machinery and thus vulnerable to overheating in warm waters, especially
during bouts of intense activity (Sharp and Vlymen, 1978). This led to tests of
tuna capacity to alter T, by adjusting retid exchange efficiency (Dizon and Brill,
1979a,b; Brill et al., 1994). Similarly, questions about tuna metabolic rate were
logical extensions of the need to develop energetics models.
It is certainly true that conjecture about tuna metabolism was strongly tied
to the generalization that tunas had a mammal-like physiology (Korsmeyer and
Dewar, this volume). It was thought that, to thermoregulate in water, tunas had to
have acquired mammal-like metabolic rates and that they had “beaten the fish
system” in the sense of having overcome the ventilatory limitations of water
(high heat capacity, low 0, volume). Stevens and Neil1 (1978) wrote, “Tunas are
not poikilotherms; at least one tuna, the bluefin, is in fact on the verge of
homiothermy.”
The bluefin studied by Carey and co-workers were very large, whereas the
kawakawa, skipjack, bigeye (ZY obesus), and yellowfin studied in the Kewalo
Basin laboratory were small (1-5 kg). Studies with these smaller tunas show that
they are not as warm as mammals, they can elevate the temperature of only certain
tissues and are thus regional heterotherms rather than true homeotherms, the heart
cannot be warmed, and they have less precise central nervous system (CNS) con-
trol over Tb (Brill et al., 1994; Dewar et al., 1994; Brill, 1996). As subsequent
sections will show, the extent to which body size is a prevailing feature in the
physiological capacity for endothermy in some species remains a largely open

question.
IV. RECENT LABORATORY STUDIES

OF TUNA ENDOTHERMY
A. Control of Heat Gain and Loss
With the discovery that bluefin and quite likely other tunas could thermoregu-
late (Carey and Lawson, 1973), the stakes were raised for physiologists interested
in tuna endothermy because they now had a model system that appeared to func-
tion like a mammal even with the limitations imposed by respiring with gills and
being immersed in water. The obvious questions were the following: How effi-
cient at heat conservation were the retia (see Section II.B.3)? Do tunas have cir-
culatory shunts that bypass retia for purposes of regulating T,? If so, are these
regulated by the CNS? How precise is tuna thermoregulation? How much heat
can RM generate?
To these ends, laboratory studies examined heat-exchanger anatomy and effi-
ciency, measured body temperature and heat balance, and determined how swim-
ming activity affects Tb and how T, affects swimming. Computer modeling of the
temperature changes exhibited by free-swimming, telemetered bluefin also chal-
lenged the ideas that a conventional thermoregulatory physiology occurred in
tunas. Neil1 and Stevens (1974) suggested that large tunas had a thermal inertia
and, rather than defending a specific Tb. simply had retarded heat gain and loss
rates that minimized changes in I’,. The next sections show how laboratory re-
search provided insight into the mechanisms of heat production and conservation
and, by permitting the substitution of real values for assumed ones, contributed
importantly to integrating tuna endothermy into fishery models.
1. STEADYSTATECONDITIONS
Heat-transfer principles applying to tunas have been elucidated by a number
of workers (Neil1 et al., 1976; Dizon et al., 1978; Sharp and Vlymen, 1978; Dizon
and Brill, 1979a; Graham, 1983; Brill et al., 1994; Dewar et cd., 1994; and also
consult the papers cited within these works). Here, we begin by defining heat
balance in a tuna swimming at steady state; that is, when its rates of heat produc-
tion (use of RM in swimming is the principal source of this heat production) and
heat loss are equal and Tb is constant (Equation 3). Under these conditions, and
assuming the gut is empty so that visceral heat generation is not contributing to
the heat-balance problem, the temperature in a tuna’s peripheral tissues ap-
proaches T,, but it has a warm core insulated by retia. Steady state heat balance
can be described by
dQ/dt = K (A/d) (Tb - T,),
where dQ/dt is the rate of heat transfer for the entire body (and which is zero at
steady state), A is body surface area, Tb is the temperature of the warm core which
has a thickness of d, and K is the coefficient of thermal exchange, an empirically
determined descriptor of heat transfer (Brill et al., 1994; Dewar et aZ., 1994).
Four aspects of this model warrant discussion. First, as emphasized in sec-
tion II.B.2, visceral as well as RM heat may contribute to steady state heat balance
in some tuna species. In this case “steady state” conditions would be subject to
change as a function of feeding frequency and the duration of the postprandial
periods required for digestion and assimilation.
Second, specification of a warm isothermal core differs from the actual tuna
condition where the “core” has a temperature gradient and its shape also varies
with RM position. In the more basal tunas the warm core encompasses the verte-
bral column and extends both horizontally and vertically. In T. obesus, T thynnus,
and I: aldungu the vertebral region is cooler than the two warm areas positioned
more laterally within the RM (Carey and Teal, 1966; Carey et al., 1971; Graham,
1973, 1975, 1983; Graham and Dickson, 1981). Thus, while models assume stan-
dard conditions in all tunas, many biologically interesting features exist because
of these interspecific differences. For example, the thermal profiles of the above-
mentioned fish might be different following a large meal. [As detailed in Graham
(1983) and elsewhere, the discrepancy between the core temperature and equation
assumptions is minor and resolved mathematically by defining a series of pro-
gressively cooler concentric rings around the central core and, with the Fourier
equation, integrating these with respect to temperature to determine an empiri-
cally verifiable thermal gradient from the core to the skin.]
Third, as developed in Graham (1983), detailed heat-transfer models include
a dimensionless term, h, describing the convective heat-transfer coefficient for
water contacting the body surface. This term may also be combined with the Nus-
selt (Nu) and Reynolds (Re) numbers to define how body shape and boundary
layer motion (velocity) affect heat transfer. These applications are beyond the
scope of this review and are probably irrelevant for tunas because they are con-
tinuously in a state of high convective flow over the body surface which minimizes
boundary layer thickness.
Fourth, K in Equation (4) describes all of the internal and external conductive
and convective properties affecting heat transfer. This includes convective heat
loss to the gills from the tuna’s warm RM core as well as “non-retial” heat-flux
avenues such as the conduction of RM (and visceral) heat from the core through
the muscle and other tissues to the body surface, and conduction of heat across
the core to other tissues and from there into the blood where it is convected to the
gills. (Note that at steady state, T, is not changing and the rate of heat loss via all
of these routes must equal heat production rate.) Because it is not possible to
4. ANATOMICALANDPHYSIOLOGICALSPECIAL17,ATIONSFORENDOTHERMY 143
simultaneously measure these different components of K, it is important to design

standardized experiments that minimize their variation, as is now discussed.
2. NON-STEADYSTATECONDITIONS
Non-steady state heat transfer applies when heat production and loss are not
equal and Tb is changing. This commonly occurs during vigorous swimming in
pursuit of prey (Figure 7) and during rapid depth changes, which can greatly in-
crease the difference between T, and T,, and even reverse the direction of heat
flow (Holland et al., 1992; Dewar et al., 1994). The non-steady state condition is
described by
dT,,/dt = K (A/d) (Th - T,) + dT, &dt, (5)
where K, A, and d are as in Equation (4), dT,/dt is rate of change of T, (“C min -I,
which can be positive or negative), and dT, MET/dt is the rate of Tb change resulting
from RM, visceral, and other sources of heat production. HPM is heat production
(“C mm’), as defined earlier. Assuming that the tuna maintains a constant swim-
32 L
31
30
3 29
e
E
3 28
ii
a 27
E
$! 26
25
24 ‘- -a ,‘cv--- ---~-%4-.-~,~~-
23
3 6 9 12 15 18 21 24
Elapsed time (min)
Fig. 7. Changes in RM (solid lines) and WM (dashed lines) temperatures of nine skipjack (Kat-
suwonus, l-2 kg) during vigorous swimming induced by chasing food thrown across a huge pool,
away from their location. The large oceanarium tank at Kewalo Basin was used and ultrasonic pulse
rate transmitters provided the temperature records. Because RM circulation is via r&z, T, increased
over the period of feeding. WM circulation is not via retiaand TWM remained about the same, although
in some specimens TwM was 0.5-2.O”C warmer than T, (23.6-23.9”C), which probably reflects probe
position in the body. (From Brill et al.. 1994. with kind permission from Kluwer Academic
Publishers.)
ming speed (and use of RM for this is the largest source of metabolic heat) and
that the thermal effects on other metabolic heat sources are minimal, the dT, MET/
dt term can be neglected (Graham, 1983; Brill et aZ., 1994). Also, because A/d is
assumed to be constant, Equation (5) reduces to
dT,/dt = K (T, - T,), (6)
and integration with respect to t yields
T, (at any time, t) = T, - [T, - Tb (at t = 0) emKt], (7)
where t is the elapsed time, T, is the equilibrium T, at the new T,, and the other
variables are as above. Studies of steady state and non-steady state heat transfer
have contributed to documentation of tuna physiological thermoregulation.
3. PHYSIOLOGICAL CONTROL OF HEAT BALANCE

The relationship between T, and Tb (usually T, and TWM)of freshly caught
bluefin provided the first evidence for thermoregulation (Carey and Teal, 1966,
1969a; Carey et al., 1971). Based on 162 temperature measurements, the linear
regression relating T, and T, was
Th = 25.84 + (0.206)T,. (8)
Thus, bluefin T,, was only slightly less in warm waters than in cool waters (Gra-
ham, 1983). Telemetric monitoring of Tb and T, provided additional evidence for
the bluefin’s capacity to control T, over a range of T,‘s (Linthicum and Carey,
1972; Carey and Lawson, 1973; Gunn and Block, this volume).
However, computer analysis of the short-term changes in bluefin T, by Neil1
and Stevens (1974) suggested that, rather than physiological thermoregulation,
thermal inertia (i.e., a large thermal mass “cushioned from T,” by conductance-
retarding retia) offered a less presumptive explanation of the data. Although
“thermal inertia” is involved in the reduced rate of heat loss in a tuna descending
into cooler water, it does not apply to the facets of tuna endothermy that require
modulation of rates of heat gain and loss in relation to T,, T,, and activity level,
including the capacity to “reverse” conductance and rapidly elevate Tb during
ascent into warmer water. Nor does thermal inertia and its assumption of a large
thermal mass strictly apply to bluefin physiology; small bluefin at a T, of 21°C
have the same T, as do giant bluefin and are warmer than either skipjack or yel-
lowfin at similar T,‘s (Linthicum and Carey, 1972, Table 1). More recent teleme-
try studies have shown that physiological thermoregulation and control of thermal
conductance occur in bigeye tuna in vivo (Holland et al., 1992).
Laboratory studies also demonstrated the capacity of tunas to change T, by
regulating K. Thermally telemetered yellowfin and skipjack tunas swimming in a
donut tank in Kewalo Basin could, within several hours of an abrupt change in T,,
alter K and arrive at a new steady state T, (Dizon et al., 1978; Dizon and Brill,
1979a,b). Because those fishes were swimming at a nearly constant velocity and
thus had stable RM heat production rates, the data suggested that changes in K
enabled them to alter T, with respect to T,. Shipboard tests also showed that
lightly anesthetized albacore exposed to abrupt cooling could alter thermal con-
ductance and reduce their cooling rate (Graham and Dickson, 198 1).
The yellowfin tuna’s capacity for altering thermal conductance was demon-
strated by Dewar et al. (1994). These tests involved imposing three successive
square-wave T, changes on steadily swimming yellowfin tuna (about 2 kg mass)
in which T,, was continuously monitored by percutaneously implanted thermo-
couples. The T, changes mimicked the rate and range of temperature change en-
countered during the fish’s normal vertical movements and were thus physiologi-
cally relevant. Furthermore, tests at higher than typical T,‘s enabled contrasting
of the impact of changes in K and temperature on T,,. The experimental tech-
nique also regulated the magnitude of each T, change so that the initial thermal
gradient between TllM and T, was always the same, thus allowing the estimates of
K to be made over the same range of TRM - T,. This also minimized the non-
r&al-regulated variables affecting K, as well as other thermal effects on physi-
ology (Brill et al., 1994; Dewar et al., 1994).
The findings were that the rate of RM temperature change depends upon T,,
T,,, and the magnitude and direction of the T, change. When swimming in 32°C
water, which is warmer than normally encountered, yellowfin respond to square-
wave cooling by immediately and rapidly shedding heat (Figure 8A). This rate of
heat loss exceeds that observed at lower T,‘s (where heat conservation would be
more important). Similarly, when the yellowtin’s T, is cooler than “preferred” and
cooler than T,, a condition is modeled that normally occurs as a fish ascends into
warm surface waters after an extended time in deeper, cooler water (Holland et al.,
1992); it heats more rapidly than if it had the approximately steady state T, of a
near-surface swimming fish exposed to a square wave of heating.
That the CNS regulates heat gain and loss is suggested by the experimental
induction of “thermal notches.” Figure 8B shows that, during the warming phase
(i.e., TRM < T,, and T, is negative), heat transfer was increased to allow the influx
of heat to augment warming. Then, when T, was dropped (T, became positive),
the fish was momentarily trapped in a “high K mode” which led to the rapid but
short-lived fall in TRM. To prevent continued heat loss at the lower T, in cycles I
and 2, heat flux was abruptly curtailed, leading to the leveling off and subsequent
increase in TRM.
The most parsimonious explanation for the rise in T,, in the “thermal notch”
is that the rapid induction of thermoconservation curtailed convective heat loss
sufficiently to elevate T,, Also, with the heat exchangers “turned off” during the
warming phase, the abrupt onset of cool water may have channeled unheated
blood directly into the yellowfin’s RM to cause localized convective cooling. Be-
cause the adjacent WM is also warm but receives less blood flow. its temperature
A
20 (0.120)
I L.r
I , . ! & . . I .,
0 100 200 300
Time (min)
T,'notch'
I / I I ,
200 250 300 350

Time (min)
would not decline as rapidly. Thus, if TRMwas less than TWM,conductive heat flux
from the WM to the RM may have also contributed to the rise in TN.
In summary, tunas do not precisely regulate Tb and thus do not thermoregulate
in the same way as mammals. Even the most refined data for large free-swimming
bluefin tunas show that they lack the thermoregulatory precision of mammals
(Carey and Lawson, 1973; Gunn and Block, this volume). Tunas do, nevertheless,
have the ability to regulate heat gain and loss and modulate K, and they do this in
concert with “thermal-gradient-altering behaviors” [e.g., changing depth (= T,),
swimming speed (= HPM), or both]. Thus, tunas appear capable of using phys-
iological mechanisms to minimize changes in Tm and other deep tissues, and they
are not prisoners of their own thermoconserving devices (see Brill et al., 1994).
The suite of physiological mechanisms underlying this remains largely un-
known. As summarized here, laboratory studies by Dewar et al. (1994), Brill et al.
(1994), and others have demonstrated that tunas do alter K, probably by adjusting
retiul heat-exchange efficiency. The anatomical studies of retia summarized above
(Section 1I.B. 1) suggest that tunas may alter K by vasodilation or vasoconstriction
of the rete blood vessels, thereby modulating blood flow through the retia and
affecting heat-exchange effectiveness. It also appears that the Z’hunnlrs species that
lack both a postcardinal vein and a central rete (Table II) may be able to adjust
T,, by altering the relative blood flow via the dorsal aorta (carrying cool blood to
the RM) and the lateral arteries. Vascular casts of the bluefin’s central and lateral
circulations (Funakoshi et al., 1983) show that arterial branches from the dorsal
aorta penetrate into the same RM regions as do retia from the lateral vessels.
Species having both central and lateral retia, in which all blood flow to the
RM presumably passes through retiu, might be able to adjust K by changing the
relative flow through the two rete types, assuming these have different heat-
exchange efficiencies. For example, Euthynnus lineatus has two small lateral retia
with relatively little surface area contact between arterial and venous vessels for
heat exchange, but a much larger central rete with a large surface area for heat
exchange (Graham and Diener, 1978; Dickson et al., 2000). However, there
are precious few details about retial geometry, vessel fine structure, and micro-
circulation in the different tuna species, and nothing is known of how rete vessel
diameter is controlled physiologically (Brill et al., 1994). There are several obser-
vations of nerves occurring near or within the retiu (Eschricht and Mtiller, 1835;
Kishinouye, 1923; Stevens et al.. 1974; Moore, 1998), but it is not known if they
innervate the rete vessel smooth muscle cells, or even if they are autonomic motor
Fig. 8. (A) Traces of T, and T,, over time in a yellowfin tuna swimming at a constant velocity.
Beginning at 120 min the fish was exposed to a series of “square-wave” changes in T,, and the effect
of these on TRM and K (parenthetic values) were calculated. (B) Traces of T, and TRM during square-
wave changes in T,. K values are in parentheses. Note that the rapid drop in T, while the tish is still
warming results in the thermal notch (see text for details). (From Dewar et al., 1994, with permission
from Company of Biologists, Ltd.)
nerves. Stevens et al. (1974) reported unsuccessful attempts to locate nerves

within the walls of central rete vessels in Katsuwonus pelamis. Apart from the
apparent capacity of bluefin to perfuse the same RM region with either warm or
cool blood (Funakoshi et al., 1983), anatomical studies have failed to show any
circulatory shunts around retia (Carey et al., 1971; Gibbs and Collette, 1967; Gra-
ham, 1973, 1975) which would provide another mechanism for controlling K.
B. Metabolic Performance
The enhancing effect of temperature on most biological rate processes was

emphasized by Carey and Teal (1966), and subsequent research has documented
this (Carey et aZ., 1971; Graham, 1975; Neil1 et al., 1976; Stevens and Neill, 1978;
Dizon and Brill, 1979a,b; Johnston and Brill, 1984; Block et aZ., 1993). Kors-
meyer et al. (1996a) provided an integrated energy budget analysis for tuna me-
tabolism in which the “enhancing effect of elevated temperature” was factored
into estimates of the different components of total metabolic rate.
First principles (Rome, 1995) dictate that elevation of TRM results in greater
RM contraction velocity, force, and power output, and a positive thermal effect
for muscle has been demonstrated at several levels. Johnston and Brill (1984)
demonstrated the positive effect of temperature on the in vitro contraction rate of
isolated skipjack tuna RM fibers. Altringham and Block (1997) showed that a
10°C temperature increase doubled the muscle contractile power output of iso-
lated blocks of RM from yellowfin tuna. Dickson (1995, 1996) found that while
the activity of the RM aerobic enzyme citrate synthase (CS) at a given temperature
did not differ significantly between tunas and their closest scombrid relatives [the
ectothermic bonitos (Sarda), mackerels @comber), and Spanish mackerels (Scom-
beromorus)], the QIOfor tuna RM CS activity ranged between 1.77 and 2.08. Thus,
when adjusted to in vivo temperatures, tuna RM has a much greater potential for
supplying energy for sustainable swimming. That temperature may also affect
scombrid swimming performance is suggested by the findings that maximal sus-
tainable swimming speed, O2 consumption rate, and net cost of transport of the
chub mackerel @comber japonicus, an ectothermic scombrid) are all higher at
24°C than at 18°C (Sepulveda and Dickson, 1998). However, what is needed to test
if endothermy enhances the swimming performance of tunas is a comparison of an
endothermic tuna with a member of its ectothermic sister taxa. A recent comparison
of swimming performance in juvenile kawakawa tuna (Euthynnus afinis) and size-
matched chub mackerel showed no interspecific difference in maximum sustainable
speed or net cost of transport (Sepulveda and Dickson, 2000). However, the kawa-
kawa in that study had a TRMthat was at most only 2.3”C warmer than T,. Similar
work on larger individuals and on bonitos is clearly needed.
Another dimension of heat conservation for tuna muscle function is that a
large percentage of the ?VM is also warm (Carey and Teal, 1966,1969a; Graham,
4. ANATOMICAL AND PHYSIOLOGICAL SPECIALIZ.ATIONS FOR ENDOTHERMY 149
1973). Tuna WM has higher activities of aerobic and anaerobic metabolic en-
zymes than that of ectothermic scombrids (Dickson, 199.5, 1996). As with RM, an
elevated T,, would positively affect contraction velocity, force, and power pro-
duction. Thus, endothermy may also have a positive effect on burst swimming and
acceleration (Graham, 1975; Dizon et al., 1978; Brill, 1996). However. no data
exist to test this hypothesis due to the difficulty of measuring burst swimming in
tunas and other scombrids. An elevated T WMand this tissue’s high aerobic activity
may also increase the rate of lactate clearance following burst swimming (Dick-
son, 1995; Korsmeyer et al., 1996a; Brill, 1996). The skipjack tuna (Kutmwonus
pelumis) has the fastest rate of lactate clearance known for any fish (Arthur et al..
1992), but no comparisons with ectothermic scombrids have been made.
The visceral cavity of four tuna species and the brains of most tunas are warm,
and this must also positively affect thermally dependent rate processes such as
digestion, gastric evacuation, assimilation, and sensory perception, although there
are no data for thermal effects on sensory perception or on assimilation (reviewed
in Korsmeyer et al., 1996a). Carey et al. (1984) documented the facultative heat-
ing of the bluefin stomach with feeding, and Stevens and McLeese (1984) found
that the bluefin’s elevated visceral temperatures resulted in a threefold increase in
the activity of digestive peptidases. It is also known that the gastric evacuation
rates of tunas (Thunnus albacares, Euthynnus lineatus) exceed those of most other
species (Schaefer, 1984; Olson and Boggs, 1986), but neither of these species has
been shown to maintain elevated TViscera. Moreover, because there are no data for
ectothermic scombrids, it is not known if the rapid gastric evacuation rates of
tunas are a consequence of endothermy. More information on the role of elevated
brain and visceral temperatures in tunas is needed.
Thus, as predicted by Carey and Teal (1966), the enhancing effect of tempera-
ture on various rate processes in tunas has been confirmed, primarily in laboratory
studies of isolated tissues. Future research to determine if such thermal enhance-
ments affect whole-animal performance, and additional data on digestion, assimi-
lation, growth, and sensory perception in tunas and their ectothermic relatives,
is needed (Brill, 1996; Korsmeyer er al., 1996a; Korsmeyer and Dewar, this
volume).
C. Tuna Locomotion, Endothermy, and Evolution
A larger issue concerning endothermy is the role it may have played in tuna
evolutionary ecology (Block et al., 1993; Graham and Dickson, 2000). Whereas
elevated temperature enhances tuna performance, the evolutionary impact of en-
dothermy may have been to expand the thermal range, both vertically and latitu-
dinally, of tunas relative to ectothermic scombrids. Because the early radiation of
tunas coincided with the geological time span in which major changes in ocean
surface currents, thermal structure, and productivity patterns were taking place,
selection that enhanced sustained swimming performance (for migration to reach

distantly located food resources) may have been important in the evolution of both
a more efficient swimming mode and endothermy (Graham and Dickson, 2000).
The paleontological record indicates that tunas diverged from a tuna-bonito
ancestor during the early Tertiary (Bannikov, 1985). At that time a number of the
physical characteristics of the modern oceans (e.g., basin geography, wind-driven
gyre circulation, thermal structure, and upwelling) were first appearing. Changing
paleoceanographic conditions may have led to the radiation of tunas from a coastal
distribution to a more open-ocean existence involving long-distance migrations.
With the cooling of ocean temperatures beginning in the Tertiary and a reduction
in the ancestral tunas’ habitat (the warm Tethys Sea), endothermy may have en-
abled the early tunas to extend their foraging to below the thermocline without
acclimating or adapting to a cold environment, in order to maintain or expand the
volume of water available for exploitation (Graham and Dickson, 2000).
We have proposed a sequence of character-state acquisitions leading to effi-
cient, high-performance swimming and endothermy in the tunas (Figure 9). This
sequence is based on the discovery that the slender tuna, Allothunnus fallai, has
its RM in the anterior and internal position that is a synapomorphy of the tunas,
and which differs from the RM distribution in the bonitos Sarda spp. and Gym-
nosarda unicolor (Graham and Dickson, 2000). We also found that the central
circulation of Aflothunnus is elaborated to form a rete-like structure composed
of numerous arterial and venous vessels to and from the RM. However, Allo-
thunnus lacks the lateral countercurrent heat-exchanging blood vessels perfusing
the RM that are present in all other tunas. Based on these characters and ances-
tral character-state reconstructions done in MacClade (Maddison and Maddison,
1992), we have proposed that the anterior, internalized RM position preceded the
evolution of endothermy (Figure 9). Block and Finnerty (1994) also proposed this
evolutionary sequence, based on some degree of RM internalization in Sardu.
Our view is that it was the selection for more efficient swimming that led to
the derived RM position of tunas. The most recent studies support this hypothesis,
because it appears that only the tunas, with a distinctly different RM distribution
in which parts of the anterior-pointing myotomal cones are composed of RM fi-
bers, swim in the thunniform mode. Recent studies of swimming yellowfin tuna
(Shadwick et al., 1999; Altringham and Shadwick, this volume) have shown that
internally placed RM produces greater strain, thus providing a selective advantage
related to swimming performance for the derived RM position. That work pro-
vides a mechanism to explain the first step in the evolutionary progression re-
vealed by our studies of Allothunnus (Figure 9). We theorized that, once RM was
internalized, elaboration of blood vessels to perfuse the RM led first to the central
rete and then to the lateral retia, which conserved enough metabolic heat for the
fish to maintain elevated muscle temperatures (Graham and Dickson, 2000). The
acquisition of endothermic capabilities would have further enhanced swimming
performance and allowed thermal niche expansion in the more derived tunas. With
TUNA-BONITO COMMON ANCESTOR
lateral, posterior red muscle position
ectothermic species
anterior, axial red muscle position
modified central circulation (rete) T
epaxial lateral arteries and veins and associated retia
red muscle endothermy confirmed
fronto-parietal fenestrae; carotid rete
1st vertebra partially fused to skull
I
hypaxial lateral arteries and veins
and associated retia
1 st vertebra fully fused to skull
reduced central rete
visceral retia
loss of central fete
r 1 i
loss of PCV
1 1
r
the Tertiary cooling of the oceans, selection for endothermy would have been very
important, and we postulate that this drove the subsequent evolution of mecha-
nisms to maintain elevated temperatures of the locomotor muscle, brain and eyes,
and viscera (Figure 9).
It is emphasized that the phylogeny shown in Figure 9 differs from the one in
Figure 2 of Collette, Reeb, and Block (this volume), which is based on cyto-
chrome b gene sequences of many of the scombrid species. If that cladogram is
supported by additional data, then the evolutionary sequence of character changes
would differ from the one we have proposed in Figure 9. Specifically, the Collette,
Reeb, and Block phylogeny requires the assumption that characters such as the
loss of a post cardinal vein and the presence of visceral retia evolved indepen-
dently in at least two clades of Thunnus. Also, because the Collette, Reeb, and
Block phylogeny does not indicate Allothunnus full& as the sister group to the
rest of the Thunnini, this would require the assumption that both changes in RM
position and a modified central circulation evolved independently in A. fallai and
the tunas or that these two characters were lost in Surdu. It should also be noted
that the position of A. fullai shown in Figure 2 of Collette, Reeb, and Block is not
r i endo- 0
Ii i t/Iermy
7 0
6 0
5
4
1 . . . . . . . ..I....
.. .. .. .. .. .
0 I
300 400 500 600
Fish FL (mm)
Fig. 10. Relationship between T,, elevation (T,) and fork length (FL) in Euthynnus lineatus
(solid circles) and two ectothermic scombrid species, the chub mackerel, Scomberjaponicus (squares;
Roberts and Graham, 1979), and the sierra mackerel, Scomberomorus sierra (diamonds; Lindsey,
1968; Dickson, 1994). A 3°C or greater T, can be generated by all E. lineatus 2 207 mm FL, the
hypothesized minimum size for endothermy (vertical dashed line). The first appearance of r&u at
95.9 mm FL (dashed line) in this species coincides with the point at which the tuna and ectotherm
curves diverge. (From Dickson ef al., 2000.)
4. ANATOMICAL AND PHYSIOLOGICAL SPECIALIZATIONS FOR ENDOTHERMY 1%
strongly supported statistically (bootstrap values are < 50%), and moreover dif-
fers from the position shown in Figure 3 of the same paper. As was reported in
Graham and Dickson (2000), an analysis of cytochrome b gene sequences from
A. fallai, Gymnosarda unicolor, and Sarda orientalis (unpublished data of Blaise
Eitner and Carol Kimbrell), combined with sequences from Block et al. (1993)
and Finnerty and Block (1995), could not resolve this node of the phylogeny.
Thus, until the problems with the molecular phylogenetic data for the Scombridae
that are discussed in Collette, Reeb, and Block (this volume) are overcome, it will
be difficult to test our hypothesis for the evolution of tuna specializations.
D. The Ontogeny of Tuna Endothermy
Juvenile tunas ranging in length from 20 to 30 mm fork length are rarely col-
lected and it has only recently been possible to study the ontogeny of endothermy.
Neither the small pelagic eggs nor the larvae of tunas have a T,; endothermy is
acquired during the juvenile stage (Dickson, 1994). The transition to endothermy
is accompanied by increases in the ability to both produce and retain metabolic
heat, and also correlates with changes in body shape (declining ratio of surface
area to volume and an increase in girth).
The studies summarized here were conducted on juvenile black skipjack tuna,
Euthynnus Zineatus, raised from postflexion larvae and early juvenile stages (lo-
20 mm fork length, FL) at the Inter-American Tropical Tuna Commission Labo-
ratory in Panama. Dickson (1994) showed that juvenile E. lineatus as small as
207 mm FL can elevate T aM 2 3°C above T, (Figure 10). Because all acute tem-
perature measurements from fishes incapable of elevating T,, at any size are
~2.7”C, Dickson (1994) hypothesized that the minimum size for endothermy in
tunas is approximately 207 mm FL.
Subsequent studies (Dickson et al., 2000) have tracked the development of
characteristics required for endothermy across this critical size. Central rete ves-
sels are first evident in E. lineatus at 95.9 mm FL, and lateral rete vessels first
appear at 125 mm FL (Dickson et al., 2000). As fish girth and mass increase, both
central and lateral retia become longer (a greater distance to the RM), and addi-
tional vessel rows are added to them (Dickson, 1994; Dickson et al., 2000). In-
creases in both rete vessel length and number augment heat retention within a RM
mass that is also increasing with fish FL (Figure 1 I).
Internal RM occurs in all juvenile tunas that have been examined, down to
14 mm FL (Dickson et al., 2000); black skipjack juveniles of this size are approxi-
mately 16 days posthatch (Wexler. 1993). The ontogeny of the unique interior-
anterior RM position of tunas has not been detailed but undoubtedly must involve
a change in fiber-type expression in the cells within the anterior-pointing cones of
the myotomes. As juvenile E. lineatus grow, total RM heat production potential
increases due primarily to increases in total RM mass (RM-body mass scaling
_-“-
25Qa-
C
zmo-
1500-
mm-
xm-
O-
0 loo 150 200 250
Fish FL (mm)
Fig. 11. Estimated total heat production potential [total activity of the mitochondrial marker en-
zyme, citrate synthase (CS), in RM] versus fish fork length (FL) in juvenile black skipjack, Euthynnus
lineatus. (A) The relationship between RM CS specific activity [international units (pm01 substrate
converted to product min-I) g-’ tissue wet weight] at 20°C and fish FL. (B) Relationship between total
RM mass and FL (C) The product of A and B is the total units of CS in the RM as a function of FL.
coefficient is 1.17) and also to a rise in the specific activity of RM CS (Figure 11).
Both of these increases with fish FL. are greater than they are in the ectothermic
scombrid Scomberomorus sierra (Dickson et al., 2000).
The size or age at which each tuna species transitions to endothermy and thus
gains some independence from the thermal environment has implications for the
early life history and ecology of the species. All tuna species spawn in warm
waters (Nakamura, 1969; Bayliff, 1980) and the juveniles may require warm wa-
ters for optimal growth and feeding, and might also not be able to exploit cooler
waters until they become endothermic. To test this idea, we need to know more
about the distribution and behavior of young tunas to determine if they must be
able to maintain a certain T, before they move into cooler waters below the ther-
mocline or at higher latitudes.
E. Endothermy in Large Tunas
Most of the laboratory studies completed to date on live tunas have used small
individuals. With the exception of at-sea studies of restrained albacore (Graham
and Dickson, 1981; White et al., 1988), these have all been done with tropical
species (Euthynnus spp., K. pelamis, and T. albacares). Thus, a major question
resulting from laboratory investigations of thermal physiology is whether the
small tunas that have been studied provide any insight into the suite of endother-
mic properties likely to be present in larger tunas. The answer is an unquali-
fied yes.
First, the initial concept held by many workers, that smaller tunas do not
normally encounter the same thermal environmental range as larger individuals,
has changed somewhat because recent tracking data for small tunas (e.g., 3- to
5-kg bigeye) show that they make excursions into very cool water (Holland et al.,
1992; Lowe et al., 2000; Gunn and Block, this volume). Field telemetry data show
that large tunas can control T, fairly well (Gunn and Block, this volume). Labo-
ratory telemetry studies indicate that l- to 2-kg tunas can also generate a large T,
during activity and maintain this for a relatively long period (Brill et al., 1994).
Although there are few data for large tunas, T, measurements on freshly decked,
large tunas suggest that they do not necessarily have a higher Tb than do smaller
individuals, but more extensive regions of the body are warm compared with
smaller tunas (Carey et al., 197 1, 1984; Linthicum and Carey, 1972). This is also
suggested by field telemetry (Gunn and Block, this volume).
While there are no metabolic data for large tunas, basic principles do suggest
properties of their thermal physiology. First, because of the allometric scaling of
metabolism and because the metabolic cost of transport diminishes with increased
body size (Schmidt-Nielsen, 1984) relative heat production should be lower in
large tunas. Also, larger tunas have lower relative amounts of RM and lower rela-
tive minimum swimming speeds (Magnuson, 1973, 1978; Graham et al., 1983).
Although these facts indicate a lower relative rate of RM heat production with
increasing size, a larger tuna has both a thicker body and a larger thermal mass.
This means that once a T, is attained, a larger tuna would take much longer to
reach thermal equilibrium at a new T, than would a small tuna. In addition, large
tunas have a more remote RM position relative to the body surface with longer
r&al vessels connecting RM to the lateral arteries and veins, a lower surface area
to volume ratio, and more insulation (subcutaneous fat)-all of which would fa-
vor a more stable T,,. Thus, although the relative size and activity of the heat
generator are smaller in a large tuna, its remoteness from the body surface and the
thermal inertia of a large body mass may lead to an expansion of the warm region
as well as a more precise regulation of Tb through a finer scale control of the
balance between heat production and heat loss (see Brill et al., 1994).
V. EFFECTS OF ENDOTHERMY ON SOME

CARDIOVASCULAR CHARACTERISTICS
This section discusses how variations in T, and T, may potentially affect two
critical elements of tuna physiology related to endothermy, cardiac performance
and the binding and transport of oxygen by Hb.
A. Endothermy and Heart Function
An account of tuna cardiovascular physiology is found in this volume’s chap-

ter by Brill and Bushnell. Tunas differ from most other fishes in having higher
heart rates and by modulating cardiac output mainly through changes in heart rate
as opposed to stroke volume. Additional research is needed to determine how
heart activity is modulated with respect to endothermy and the metabolic require-
ments of the RM. The tuna heart is essential for endothermy, but it is not warm
[i.e., it is seldom warmer than O.l”C above T, (Carey et al., 1971; Graham, 1983)]
and there are no known excitation-contraction coupling specializations to mitigate
the effect of acute temperature change on heart rate.
Korsmeyer et al. (1997a) documented a rapid and strong effect of T, on the
heart rate of steadily swimming yellowfin. A T, decrease from 28 to 18°C reduced
heart rate by about 50%, and even though the stroke volume of the slowed heart
increased, cardiac output declined by about 30%. Rapid depth changes expose
tunas to abrupt T, changes (as great as 8- 14°C in a few minutes for ?? obesus;
Holland et al., 1992). The Korsmeyer et al. data indicate how such a change would
affect the heart: as T, declines so does T HEART and cardiac output. However, as
detailed in Section IV.A.3, TRM would “be defended,” and RM would cool at a
much lower rate. Thus, cardiac output to RM would drop abruptly while RM 0,
demand (a function of velocity and TRM) would remain relatively constant (Kors-
meyer et aE., 1997a,b).
The mismatch between blood-perfusion rate and RM 0, requirements result-
ing from a rapid T, change might limit the capacity of a tuna to remain in cool
water. On the other hand, slowing of the heart could actually favor maintenance
of T,, and thus lengthen the tuna’s time limit in cool water. The key issue in the
perfusion reduction is how tissue 0, delivery is impacted. Korsmeyer et al.
(1997b) reported that yellowfin tuna swimming in a water tunnel (normoxic water
at 25°C) had a mean venous 0, content of about 50% of arterial concentration.
Thus, a sizable venous 0, reserve is available to the tissues. As the rate of blood
flow through RM capillaries falls in cooler water, the RM and other warm tissues
could obtain their required 0, by utilizing the venous reserve. This means that,
provided cardiac output is adequate to sustain the O2 reserve, tissue aerobic me-
tabolism could be maintained. In fact, it might even be the case that under such
conditions the potential for heat retention within RM increases (i.e., K is reduced).
If a greater quantity of 0, is used (and more heat is produced) per unit volume of
blood flow, the ratio of heat removal to heat production is reduced, thus lowering
convective heat transport from the RM. A lower perfusion rate also means that
blood residence time within the retiu increases, and this favors countercurrent heat
transfer. A calculation could, for example, be made to determine the extent to
which the heart-rate changes observed by Korsmeyer et al. (1997a) could account
for the reduced K values observed for cooling yellowfin by Dewar et al. (1994).
Endothermy is critically dependent upon blood flow and, because T, changes
have a direct and immediate effect on the heart, cardiac output makes an important
contribution to heat balance. This, however, does not mean that the T, effect on
the heart is the only or principal mechanism underlying the modulation of K.
While thermal disequilibrium resulting from changes in T, can result in blood-
flow changes that appear to augment heat balance (i.e., slowing the heart in cool
water, and accelerating it in warm water), changes in heat-balance requirements
also occur independently of T,. For example, increased swimming speed will re-
quire an elevated cardiac output, mediated by either catecholamines or sympa-
thetic stimulation, and T, usually increases (Dewar et al., 1994; Brill et al., 1994).
It is unknown how increased velocity in cooler water would affect heart action
and, in some environments, a deep-swimming tuna will also come in contact with
hypoxic water. It can be expected that, whereas cardiac function may be respon-
sive to Tbr control of the heart for purposes of 0, delivery will prove of greater
importance than heat balance.
B. Endothermy and Hb-0, Affinity
Endothermy also has implications for the kinetics of 0, binding by Hb. Stud-
ies with a diversity of tuna species have documented the temperature indepen-
dence of tuna Hb-0, binding (Carey and Gibson, 1983; Brill and Bushnell, 1991;
Lowe et al., 2OOO), an adaptation that permits rapid changes in T, without
impacting 0, transport.
However, circulation through the countercurrent heat exchangers poses an-
other potential problem for tuna Hb. Blood reaching thermal equilibrium with
water in the gills may be transported to tissues having the same temperature as T,
or a higher temperature. In the latter case, the blood undergoes a relatively large
temperature increase and remains warm until it passes back through the reticr.
Blood heated within the retia cannot equilibrate with the atmosphere (i.e., it is a
closed system) and, although its total O2 and CO, content does not change, heating
affects the pH and the gas solubility of the plasma, which results in changes in
POZ, PCO*, and pH.
There has been considerable uncertainty over what adaptive scenario best ap-
plies to the closed-system temperature changes imposed on tuna Hb. The normal
response to heating is for the I-%-O, binding curve to shift to the right (i.e.,
Hb-OZ binding affinity is reduced, which raises the PO, and thus the 0, diffusion
gradient). After the first discovery of temperature-independent 0, binding for
bluefin tuna Hb solutions (Rossi-Fanelli and Antonini, 1960), it was argued that
no effect or a negative effect of temperature on Hb-0, affinity was necessary to
prevent the premature off-loading of 0, within the retia (which would raise the
trans-refiul PO, gradient), and that a reduction in Hb-O2 afhnity within the rete
would not favor tissue gas exchange (Graham, 1973; Carey and Gibson, 1983;
Cech et aZ., 1984). It was further assumed that because Hb insensitivity to tem-
perature was critically important for tissue metabolism, the conditions for gas
transfer in the gills (high surface area, short diffusion distance, high perfusion and
ventilation) and in the RM (a strong Bohr effect) would ensure efficient gas ex-
change (Graham, 1973; Cech et al., 1984).
When exposed to closed-system heating, the Hb of both bluefin and albacore
tunas undergoes a reversed temperature effect (i.e., affinity increases; Carey and
Gibson, 1983; Cech et uZ., 1984), whereas the Hb of the skipjack tuna is unaffected
by closed-system heating (Sri11 and Bushnell, 1991). On the other hand, normal
(right-shift) responses to closed-system heating have been shown for yellowfin
and kawakawa tunas (Jones et al., 1986; Brill and Bushnell, 1991) and for the
bigeye tuna (Lowe et al., 2000). If a Hb molecule leaving the gills does not enter
a part of the tuna body where temperature increases, there is no need for an intrin-
sic Hb property that compensates for closed-system heating. Taken together, these
findings suggest no correlation between endothermy and closed-system tempera-
ture changes, and the topic needs further study.
VI. SUMMARY, CONCLUSIONS, AND FUTURE

DIRECTIONS FOR LABORATORY STUDIES
Temperature is a critical ecological factor, particularly for aquatic organisms.

That fishes are in general ectothermic (i.e., T, = T,) has been recognized from
the time of Linnaeus. That tunas are warmer than T, and the anatomical basis for
heat conservation were both discovered over 160 years ago, which qualifies tuna
endothermy as one of the oldest subject areas within the field of comparative
physiology. In the mid- 1960s when comparative physiology was gaining momen-
tum, publication of the first electronic measurements of tuna T, and Carey and
4. ANATOMICAL AND PHYSIOLOGICAL SPECIALIZATIONS FOR ENDOTHEKMY Is!,
Teal’s (1966) elucidation of the biophysical, anatomical, physiological, biochemi-

cal, and biological problems inherent in tuna endothermy established this subject‘s
core importance. New initiatives in the study of tuna endothermy were aided by
the timely completion of a robust classification system for the tunas and for the
entire scombrid family. These works also documented important comparative fea-
tures of the tuna vascular heat-exchange system and provided details about the
distribution and natural history of different species. Novel information about
scombrid morphology and locomotion biomechanics provided the link between
the warm temperatures of tunas, their vascular anatomy, and high activity rates.
Thus, works by Kishinouye, Carey and Teal, Gibbs and Collette, Fierstine and
Walters, and others have become keystones for understanding the evolutionary
history of these specializations and the functional significance of tuna endo-
thermy. Added momentum for laboratory studies of tuna thermal biology at Ke-
walo Basin came from theoretical models suggesting that the distribution and
abundance of tunas could be predicted from ambient temperature and oxygen con-
ditions and that tuna T, and metabolic O2 requirements might limit their occur-
rence in certain waters.
In the last two decades, many advances in our understanding of endothermy
in tunas have occurred as a result of laboratory studies, but there is still much to
be learned:
1. It has been established that tunas do, indeed, control their thermal conduc-
tance and alter heating and cooling rates, depending on environmental tem-
perature and swimming speed. What we still do not know, however, is how
this control is achieved. It is hypothesized to be due to physiological con-
trol of heat-exchanger effectiveness, by contracting or relaxing the smooth
muscle in the countercurrent heat exchanger blood vessel walls, but how
this is mediated remains unknown.
2. The enhancing effects of increased T,, on RM contraction rate and power
output and of increased TVIScERA on digestive enzyme activities have been
demonstrated. However, how or if these thermal effects translate into in-
creases in whole-fish performance as a result of endothermy has not been
substantiated, due to the difficulties of testing such hypotheses with live
tunas in the laboratory. The role of visceral heat production clearly impacts
both steady and non-steady state models of heat transfer, and data are
needed in order to estimate this effect. Also, we need data on how velocity
changes, whether spontaneous or induced by T, or other factors, alter
heat balance. Finally we lack comparative data for similarly sized speci-
mens of the tuna sister taxa, the bonitos and mackerels, with which to make
valid comparisons for performance enhancements actually associated with
endothermy.
3. Recent laboratory studies, combined with modern methods of phylogenetic
analysis and reconstruction, have resulted in the mapping of characters re-
lated to locomotion and endothermy onto phylogenies of the family Scom-

bridae. These have led to a hypothesized series of character-state acquisi-
tions in the ancestral tunas that led to the evolution of endothermy, which
will guide and focus future research into this question. We have only
a limited understanding of the significance of interspecific differences
among the tunas, and future studies should seek to elucidate the diversity
of adaptations and endothermic capabilities of these fishes and their closest
relatives.
4. The first studies of the development of endothermy in tunas have been con-
ducted, but these have been based almost exclusively on individuals raised
in captivity. There is a need to repeat these studies with wild-caught juve-
nile tunas, if they can be found. Future study of species such as bluefin and
albacore that are known to inhabit cool waters as adults will be important
in determining how the ontogeny of endothermy impacts tuna ecology and
life history.
5. Specific effects and consequences of endothermy on the cardiovascular
system have been described. Additional studies are needed to explain inter-
specific differences in the effects of temperature on Hb-0, binding. It is
also important to understand more fully the consequences of regional het-
erothermy for tunas, given that the heart’s temperature cannot be main-
tained above T, .
The past decades have seen a great deal of activity and progress in the field
of tuna physiology and endothermy. Future integrated laboratory and field studies
designed to complement one another will lead to a broader understanding of size
effects, of the consequences of the many interspecific differences among the
15 species of tunas, and of the evolutionary radiation of tunas.
ACKNOWLEDGMENTS
Research leading to this review has been supported by grants from the U.S. National Science
Foundation (IBN 93-18065 to K.A.D, and IBN 93-16621 and 96-04699 to J.B.G). Support was pro-
vided by the intramural grant program at California State University, Fullerton (K.A.D), by the Aca-
demic Senate, University of California, San Diego (J.B.G.), and by the Japanese Society for the pro-
motion of Science (J.B.G.). We thank B. Block, E. D. Stevens, and one anonymous reviewer for their
comments on the manuscript.
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5
ADVANCES IN ACOUSTIC, ARCHIVAL,

AND SATELLITE TAGGING OF TUNAS
JOHN GUNN
BARBARA BLOCK
I. introduction
II. Acoustic Tagging
A. Technology and Methods
B. Tracking Studies of Tuna
C. Summary
III. Archival Tags
B. Archival Tagging of Tunas
C. Summary
IV Pop-Up Satellite Tags
B. Application of Pop-Up Satellite Tags on Tunas
c. summary
V. The Problem of Attachment
VI. The Future of Acoustic, Archival, and Pop-Up Satellite Tagging
A. Technology
B. The Future Application of Electronic Tags
and Integration of Data into Spatial Dynamics Models
I. INTRODUCTION
In the scientific and popular literature, tunas are most often described ashighly
migratory fishes-“wanderers” of the world’s oceans. Their “highly charged life-
styles as apex predators in the oceanic pelagic environment” (Dickson, 1995) are
facilitated by a number of anatomical, biological, and physiological specializa-
tions (Brill, 1996; Bushnell and Jones, 1994; Sharp and Dizon, 1978).
While considerable time has been spent in the laboratory examining the phys-
iological attributes of tunas, relatively little attention has been paid to critical
shortcomings in our understanding of what tuna do in their open ocean environ-
167
T”ruA Volume IV Copyright 0 2001 by Acadenuc Prrss
FISH PHYSIOLOGY All rights ot repnduction in any torm re*erwd
168 JOHN GUNN AND BARBARA BLOCK
ment. For example, although most species of tuna are capable of long-distance
movements, there is growing evidence that for some species or populations large-
distance migrations are more the exception than the rule (Hampton and Gunn,
1998; Hilborn and Sibert, 1988).
Hunter et al.‘s 1986 review of tuna movement dynamics concluded that for
many of the tuna species major uncertainties regarding the nature and extent of
movement constrained stock assessments and the management of resources that
are often shared by many countries. The most serious of these uncertainties
were the:
1. Timing, extent, directionality, and seasonality of movement
2. Rates of exchange of exploited adults among different management juris-
dictions
3. Rates of exchange among vertical and horizontal habitats fished by differ-
ent gears
4. The distribution of adults
5. Residence times and probability of return
6. Links between environmental factors, movements, and distribution
Since Hunter et al.‘s review, the world’s tuna catch has increased by almost
30% (FAO, 1998), and populations of albacore, bigeye, southern bluefin, and At-
lantic bluefin tuna in various ocean basins have been listed by the IUCN in their
Red List of endangered species (Hilton-Taylor, 2000) under categories ranging
from vulnerable to critically endangered. Increased exploitation and scrutiny of
stock assessments has resulted in increased pressure on fishery scientists and man-
agers to reduce uncertainty in stock assessments and reduce the risks of overex-
ploitation of tuna populations. However, despite their very significant commercial
value, and the status of some tuna populations, many of the uncertainties identi-
fied by Hunter et al. (1986) remain as unresolved today as they were 15 years ago.
Hunter et al. (1986) made recommendations on “actions needed to improve
the knowledge of tuna movements.” These were to:
1. Establish international arrangements whereby data on tuna movement
could be shared
2. Increase the number and kinds of observations of tuna movement in the
vertical plane
3. Develop and use technology for tracing the actual paths followed by
tuna over extended periods and for measuring movements independent of
fisheries
4. Conduct intensive studies on tuna movement dynamics which combine old
and new technologies
How have we progressed since 1986.~
Regional tuna management agencies are now established, or are in the final
stages of being established, to conserve most of the world’s tuna resources. This
5. ADVANCES IN TAGGING OF TUNAS 169
is an important advance that provides a good basis for sharing data on tuna
movement.
Research into tuna movement and migration has also benefited immensely
from the development of new technologies-including a suite of electronic tags,
satellite communication and remote sensing, and faster computers. As a result,
there has been significant progress in Hunter et al.3 second and third “actions.”
The focus of this chapter is to review the advances in tagging technology since
1986, and the ways in which these new technologies in combination with recent
acoustic tracking have provided exciting new insights into tuna movement, behav-
ior, and physiology in the open ocean.
For some species, we are finally beginning to understand where tuna go and
what they do in their open ocean, pelagic environment. The rapid advances made
over the last 5 years suggest it may not be too long before integration of three-
dimensional movement data into spatial dynamics models is actively pursued.
As many of the new tagging technologies are still under development or in
early stages of application, we have integrated a review of the recent literature
with a broad range of observations from our unpublished data. In so doing we
hope to provide a benchmark and assist in the optimal use of the many exciting
new technologies available.
II. ACOUSTIC TAGGING
The first published account of the acoustic tracking of tuna is that of Yuen
(1970) who used acoustic tags to study the movement and behavior of skipjack
off Hawaii in August 1969. Twenty days earlier Carey and Lawson (1973) had
apparently been the first to track tunas when they began their pioneering work on
Atlantic bluefin off the coast of Nova Scotia. Yuen (1970) used 8-cm-long, 50 kHz
transmitters, weighing 62 g in air, in conjunction with a frequency-modulated so-
nar on board the research vessel Townsend Cromwell. His technology, crude as it
was in comparison to many of today’s systems, provided signals at ranges of up to
2.3 km and allowed him to examine die1 shifts in the position of his fish relative
to topographic features. Carey and Lawson (1973) used acoustic telemetry to
study the physiology of giant bluefin, and by the time Hunter et al. (1986) wrote
their review, acoustic or sonar tags had been used successfully to study the fine-
scale movement, thermal physiology, and behavior of individuals of a number of
species of tuna [skipjack (Dizon et ul., 1978) albacore (Laurs et al., 1977), yel-
lowfin (Yonimori, 1982; Carey and Olson, 1982) and Atlantic bluefin (Carey and
Lawson, 1973)].
In the early tracking work a key issue was whether the behavior of a tracked
animal was normal, or whether it was affected by stress caused by handling and/
or capture. The labor-intensive nature of tracking had also meant that observations
were generally from a relatively narrow size range and thus it was unclear whether
the promising results could be extrapolated to either larger and more mature fish in
the case of yellowfin and bigeye, or smaller fish in the case of Atlantic bluefin. Con-
siderable effort has been placed into acoustic tracking over the last decade, and to
some extent these uncertainties have been addressed and some of the gaps filled.
The design concept for ultrasonic acoustic tags has changed little since the
work conducted by Yuen (1970) and Carey and Lawson (1973)-ultrasonic fre-
quencies are generated by driving an annular ceramic transducer at its resonant
frequency, and the frequency of the signal transmitted is determined by the trans-
ducer diameter. However, acoustic tag technology has progressed significantly
throughout the last decade. As electronic circuitry controlling tag function has
been miniaturized with surface mounting and then integrated circuit technology,
tags have become smaller. The constraints of transducer size and battery volume
remain when long range or extended transmission life is required. A number of
new sensor options have been introduced that enhance the ability of researchers
to study movement of tunas in three dimensions, physiology, and behavior. For
example, Vemco Pty., Ltd., of Nova Scotia Canada supplies tags with sensors that
collect data on depth, temperature, heart rate, and swimming speed (paddle wheel
sensor). Used in combination with real-time measurements of the physical and
biological environment, acoustic tags have become a powerful tool in examining
environmental preferences of tuna (Block et al., 1997; Brill et al., 1999; Dagorn
et al., 2000). Acoustic studies primarily focus on collecting data from a single fish
equipped with the ultrasonic tag. The tag encodes the data as a series of ultrasonic
pulses transmitted through the water column to a hydrophone and receiver on the
ship. Few studies on tuna have been designed to acquire data from more than one
sensor at a time. To record two types of data from a single fish simultaneously
requires using two tags of different frequencies, or a multiplex acoustic tag such
as a pressure and temperature device, or a pressure, ambient temperature, and
swimming speed tag (Block et al., 1992).
The recent development of multidirectional hydrophone arrays coupled with
independent acoustic receivers and computers has improved estimation of direc-
tion and range of fish relative to the tracking vessel (Block et al., 1997), and per-
haps just as importantly have made the very labor-intensive task of following fish
for hours to days much easier on the researcher.
“Listening stations” are an exciting new acoustic technology. They are acous-
tic receivers that are moored at set locations, and are able to communicate with
and log details of tags that come within range over very extended periods of time.
Although listening stations have yet to be fully evaluated for tunas and other oce-
anic pelagics, a recent study on yellowfin tuna (Klimley and Holloway, 1999)
demonstrated their use in examining school fidelity and the residency of fish
around Fish Aggregating Devices (FADS). To date, the most extensive work with
5. ADVANCESINTAGGINGOFTUNAS 171
listening stations has been on salmonids (Lacroix and Knox, 2000) have used
arrays of listening stations in enclosed embayments to examine migratory behav-
ior and residency of fish.
The success of listening stations has spawned the development of “chat tags,”
which combine many of the features of archival tags (see below) with acoustic
transmission of data when a fish comes near enough to a receiver. The receiver
used with chat tags regularly sends signals out to search for and identify tags
within its range. Having received a positive response from a tagged fish, it sends
a command enabling the tag to download data via an acoustic signal (VEMCO,
2000). Although “chat tags” have yet to be used on tuna, they have great potential
in areas where fish are likely to return regularly to topographical or aggregating
features.
B. Tracking Studies of Tuna
Six species of Thunnus have been acoustically tracked since Yuen’s (1970)
early work on skipjack-Atlantic bluefin (1: thynnus), Pacific bluefin (I: o&n-
talk), southern bluefin (I: muccoyii), yellowfin (I: albacares), albacore (r alal-
unga), and bigeye (I: obesus). Recent efforts have been directed toward broaden-
ing the size range of fish on which observations are being made to include adults,
for example, Brill et al. (1999) in yellowfin, and Dagorn et al. (2000) in bigeye,
and significant work has been undertaken on simultaneous measurement of envi-
ronmental variables while tracking (Block et al., 1997; Josse et al., 1998; Brill
et al., 1999; Dagom et al., 2000; Marcinek et al., 2001).
1. YELLOWFIN
Yellowfin tuna (T ulbacares) have been tracked more than any other tuna spe-
cies. The literature describes tracks of 23 fish, ranging in size from 54 to 167 cm
fork length (FL). The duration of these tracks ranged from 4 to 86 h, and in total
63 1 hours (approximately 26 days) have been observed.
All tracking data suggest that yellowfin, in coastal and open ocean habitats,
are primarily inhabitants of the mixed layer. Although they are obviously capable
of swimming to great depths-Carey and Olsen (1982) followed one fish that
descended to 464 m-yellowfin spend most of their time in the upper 100 m
above the thermocline. The most likely explanation for their limited depth distri-
bution appears to be an inability to cope physiologically with temperatures below
the thermocline. The same factor would explain their geographical distribution
within tropical and subtropical latitudes. Even at large sizes, where surface area
to body mass ratios and a vascular countercurrent heat exchanger allow mainte-
nance of elevated body temperatures, it appears that water temperature limits the
cardiac muscle function and hence restricts vertical movement (Still et al., 1999).
Brill et al. (1999) found that in Hawaiian waters, where sea surface temperatures
172 JOHNGUNNANDBARBARABLOCK
(SSTs) were 24°C the maximum dives of large yellowfin appeared to be limited
by a temperature differential of 8°C below sea surface temperature. In these fish
the maximum dives were to 250 m. At the northern extent of their range in the
eastern Pacific, yellowfin occupy waters with SSTs of 19-20°C and in this habi-
tat small yellowfin are primarily restricted to waters above the upper thermocline
(18-45 m) and temperatures of >17S”C (Block et al., 1997).
In many cases, the objective of tracking has been to understand the behavior
of yellowfin around fish aggregating devices and topographic features (Yonimori,
1982; Holland et al., 1990; Cayre, 1991; Cayre and Marsac, 1993; Klimley and
Holloway, 1999). Very similar patterns of behavior have been observed for small
yellowfin (40-100 cm FL) associated with FADS in the Pacific (Hawaii) and In-
dian oceans (Seychelles; Holland et al., 1990; Cayre, 1991). In both locations, fish
have shown very close associations with FADS and other topographic features
such as sea mounts and continental shelf edges, and there has been clear diurnal
variation in their position relative to these features and their depth preferences.
Holland et al. (1990) were able to show that yellowfin off Hawaii stayed close to
FADS or the continental shelf drop-off during the day, while during the night they
tended to move away from these features. Klimley and Holloway (1999), using
fixed listening stations in the same area, found that individuals tended to revisit
FADS regularly, and often remained in the same school in which they had been
tagged days to months previously. Their data, showing an allegiance to a school,
a tendency for fish to return to the site at which they were tagged, and a set tem-
poral pattern for revisiting sites, led Klimley and Holloway (1999) to hypothesize
that their yellowfin had migratory pathways, consisting of “waypoints,” that were
visited regularly. The hypothesis is intriguing, and serves to emphasize the value
of data collected over long periods. It would have been extremely difficult to make
the observations on which the hypothesis is based on tracking data alone.
Oscillatory diving is a behavior observed frequently in yellowfin tracking
studies (Carey and Olsen, 1982; Holland et al., 1990; Block et al., 1997). In this
mode of swimming, ascent rates are higher than descent rates. Several authors
have suggested that the tuna glide during the descent, a behavior that would result
in significant energy savings (Weihs, 1973). Although gliding has yet to be con-
firmed in the open ocean, recent success with acoustic electromyogram tags on
captive tuna (Dewar et al., 1999) suggests that it should be possible to examine
muscle activity in wild fish. If it could be demonstrated that swimming muscle
activity decreased significantly during descent, the hypotheses based on tracking
data could be validated.
2. BIGEYE
Twelve bigeye tuna tracks are reported in the literature for fish ranging in size
from 57 to 160 cm [length estimated from the weight of approximately 70 kg
given by Carey and Lawson (1973)]. The tracks range in duration from 6 to 29 h
(average = 19 h), and in total 228.5 hours have been observed. Carey and Lawson
(1973) were the first to track bigeye when they double tagged a large adult off the
New England coast of the USA with both stomach and water temperature tags,
and followed it for 17 h. On the basis of their limited observations, and compari-
sons with tracks of Atlantic bluefin made with similar equipment, they concluded
that bigeye did not appear to control their body temperature. In the late 1980s
Holland began his important research into bigeye movement and thermoregula-
tion, based on tracking data. He demonstrated the very different depth distribution
of yellowfin and bigeye (Holland et al., 1990). Of particular interest were the
observations that although the geographic ranges of these species overlap signifi-
cantly, and that they share an association with FADS and floating objects, tracked
bigeye differed from yellowfin in that they regularly made extensive and pro-
longed excursions below the thermocline as part of die1 vertical migrations.
Tracking data suggest that bigeye are generally found in the mixed layer during
the night, while during the day they regularly dive to depths in excess of 200 m.
Small (3 -5 kg) bigeye appear to be restricted to depths above the 15°C isotherm
(Holland et al., 1990), whereas adults are capable of much deeper diving, and
regularly make prolonged excursions to 500+ m during the daytime as they fol-
low the deep scattering layer (Holland et al., 1992; Josse et al., 1998; Dagorn
et al., 2000). At these depths, bigeye spend significant time in water temperatures
as low as 7°C and tracking data have revealed the species’ unique behavioral and
physiological adaptations to thermoregulation in these temperatures (Holland
et al., 1992; Holland and Sibert, 1994). Although based on very few observations,
tracking has demonstrated how bigeye are able to take advantage of a much
broader foraging space than yellowfin. They have the ability to forage in both the
warm mixed layers of tropical and subtropical latitude and the cooler waters well
below the thermocline at subtropical and warm temperate latitudes.
3. BLUEFINS
There has been relatively little tracking of the three bluefin tuna species since
the pioneering work on the thermal biology of Atlantic bluefin by Carey and
Lawson (1973), Carey et al. (1984), and Stevens et al. (2000; based on data col-
lected by Carey in 1978). Carey’s research, using acoustic tags fabricated in his
laboratory, demonstrated the capacity of giant Atlantic bluefin to thermoregulate
through significant ranges in ambient temperature. At water temperatures varying
between 9 and 17’C, the muscle temperature of giant bluefin held in large pens
remained at about 24°C (Stevens et al., 2000). Using acoustic tags placed in the
stomach, Carey et al. (1984) also made the first observations of significant visceral
warming following a meal, and based on these data suggested that the elevated
temperatures would serve to speed digestion and allow the tuna to feed frequently
when food is abundant.
Lutcavage et al. (2000a) tracked 12 adult Atlantic bluefin (136-340 kg)
in the Gulf of Maine off the northeast coast of the USA to obtain information on
surfacing behavior for use in interpretation of fishery-independent aerial surveys
of abundance. During tracks of 3.5-48 h (average 28 h) the bluefin remained
largely in the upper mixed layer (mean swimming depth was 14 m). However, less
than 8% of this time was spent on the surface. Although mean swimming speed
over the ground was 5.9 km h-l, speeds of 20-31 km h-’ were observed for brief
periods. Perhaps the most significant feature of the data collected by Lutcavage
et al. (2000a) was the fact that the tagged fish remained in schools throughout the
tracking periods, allowing the study to infer the behavior of schools rather than
just individual fish (as is usually the case in tuna tracking data). The association
of tagged fish with their school was achieved by attaching transmitters to free-
swimming fish using a harpoon attachment technique (Chaprales et al., 1998).
Davis and Stanley (in press) have recently reported on tracking studies of the
vertical and horizontal movement of juvenile southern bluefin tuna (SBT) in the
Great Australian Bight. They tracked 16 SBT ranging in size from 67 to 103 cm
(FL), for periods of between 1 and 49 h (average 16.5 h). Like Lutcavage et al.
(2OOOa,b,c),the objective of their work was to examine the surfacing behavior of
fish to determine the probability of sighting SBT schools during aerial surveys.
Davis and Stanley (in press) found that in the continental shelf waters of the Great
Australian Bight, juvenile SBT spent long periods throughout the day on the sur-
face, and horizontal movements were commonly between topographic features
such as reefs, islands, and the shelf break.
Recent work on Pacific bluefin tuna (Marcinek et al., 2001) provides tracking
and physiological data on 2- and 3-year-old fish in the eastern Pacific. Six Pacific
bluefin tuna were tracked for a period of 46 - 86 h with both depth and temperature
transmitters. These data suggest they are similar in many ways to their very close
relative, the Atlantic bluefin. Figure 1 shows 4 days in the life of a Pacific bluefin
(9801) equipped with two acoustic tags transmitting pressure and deep slow-
oxidative muscle temperature information. The data are shown in relationship to
the thermal stratification of the water column as determined with a CTD. Pacific
bluefin as well as Atlantic bluefin examined with similar acoustic techniques
(Carey and Lawson, 1973; Lutcavage et al., 2000) show a preference for the sur-
face and mixed layer. On several occasions Pacific bluefin 9801 spent extended
periods at depth in cooler waters, as well as periods during the afternoon at the
surface. The acoustic tracking data indicate that Pacific bluefin tuna spent the ma-
jority of the time in the warmest parts of the water column in the region of the
eastern Pacific where the study was conducted. Direct observation of the internal
muscle temperatures of the Pacific bluefin tuna revealed a relatively constant
muscle temperature with a range from 23 to 26°C. These values are similar to data
from muscle temperature data obtained from Atlantic bluefin tuna by Carey and
Lawson (1973).
0 30
20 6
e
P
J 40 %
g 60 25 g
c, E
8Q 80 g
100 6.
G
120 20
16:00 20:oo 0:oo 4:Oo 800 12:oo 16:00
7/10/98 7111196
0 30
20 B
e
P e!
2 40 3
g 60 25 g
c
g 80 E
0
100 g
2
120 20
16:00 20:oo 0:oo 4:oo 8:OO 12:oo 16:00
7/l
20
Fi
g! 40
5 60
f
0 80
n
100
16:OO 20:oo 0:oo 4:oo a:00 12:oo 16:00

7/12/98 7/13/98
9801
20
P
9 40
E 60
c
E 80
0"
100
16:00 2000 0 00 4:oo a:00 12:oo 16:00

7/13/98 7/14/98
Time
Fig. 1. Four days in the life of a Pacific bluefin tuna, Thunnus on’enralis, equipped with two
acoustic tags measuring pressure and muscle temperature. These data are overlaid on data showing
the thermal structure of the water in which the fish was swimming obtained with a Conductivity,
Temperature, Depth Recorder (CTD). Marcinek er ~1.. 2001).
4. ALBACORE
Laurs et al. (1977) tracked albacore in the North Pacific, and found they un-
dertook frequent vertical migrations during both day and night. Their study was
also important as it was one of the first to demonstrate the importance of frontal
systems in the movement patterns of tunas-similar observations were later to be
made for yellowfin (Holland et al., 1990; Block et al., 1997; Brill et al., 1999) and
Atlantic bluefin (Lutcavage et al., 2000a). In the case of albacore, tracking data
showed they tended to aggregate and move along the warm side of fronts, pre-
dominantly in waters above 15°C. Recent albacore tracking data indicate that they
have a conspicuous presence at the thermocline, and appear to remain out of the
mixed layer much of the time (B. Block, unpublished data).
C. Summary
Acoustic tracking has provided significant contributions to our understanding

of the behavior, localized movement, and physiology of six 7’hunnus species.
Specifically,
l Tracking has been instrumental in providing the first examination of fine-

scale horizontal and vertical movement patterns of tunas in a range of habi-
tats, and in particular oceanographic frontal zones.
l Tracking data have provided baseline information on the thermal and depth
habitat preferences for at least a few individuals of all six species of Thun-
nus. For yellowfin and bigeye the data are extensive enough to examine
changes in these parameters with body mass.
l Acoustic tags have been used to acquire thermal physiology of muscle
temperature on Atlantic bluefin, Pacific bluefin, and bigeye tuna; visceral
temperatures of Atlantic bluefin; and swimming speeds of albacore, yellow-
fin, bigeye, Atlantic bluefin, Pacific bluefin, and southern bluefin.
l Tracking data have also provided descriptions of the nature and extent of
association of yellowfin, bigeye, and southern bluefin tuna with FADS and/
or topographic features.
Unfortunately, we do not have enough tracking data for any species to define
lunar, seasonal, interannual, ontogenetic, or regional differences in their behavior,
habitat preferences, and physiology. If acoustic tracking data are to be a useful in-
put into movement and spatial dynamics models developed as components of stock
assessments, then understanding the nature and extent of temporal variation in pat-
terns of behavior and movement is a very important goal for future research. In the
spatial context, we are limited somewhat in our ability to extrapolate from the ex-
isting acoustic tracking data as the majority of these have been collected from fish
swimming close to islands or continental land masses. Without comparable data
5. ADVANCES IN TAGGING OF TIJNAS 177
for fishes in open ocean habitats, it is not possible to objectively determine

whether the behavioral observations made to date are representative of the species
or are habitat-specific.
Quite simply, the requirement to continually follow a fish with a research ves-
sel is the major limitation of acoustic telemetry. Acoustic tracking also requires
intensive effort on behalf of the researchers and ship crew to stay with the fish on
a 24-h basis, and often can be limited by human endurance. The costs involved in
tracking have limited the sample sizes and meant that most observations have been
short term-l to 4 days. Although there are undoubtedly unpublished tracking
data we have not covered here, the total number of tuna tracked since Yuen’s
(1970) first work with skipjack is less than 60, and there have been less than
120 days of behavior observed.
Most acoustic tracking has involved the release of a single fish caught on hook
and line, and there is some question whether the behavior observed represents
school-associated behavior. However, more recent work has focused on tagging a
single fish while in a school (Lutcavage et al., 2000a; Davis and Stanley, in press)
or releasing a school of fish simultaneously with the individual tuna equipped with
tags (Marcinek et al., 2001).
The maximum distance between the vessel and the fish that has been reliably
achieved for tracking is 0.7 NM (nautical mile), and most often the distance is
0.25-0.5 NM. Thus, the question of how the close proximity of a tracking vessel
may affect behavior of tuna has been a concern for tuna researchers for many
years. For example, Davis and Stanley (in press) found some fish were attracted
to their vessel and to other fishing vessels in the area. To objectively answer the
attraction/repulsion and stress questions simply through further tracking seems
circular, although tracking for longer periods-perhaps 5-7 days-may allow
resolution of whether behavior changes over time. Some experienced trackers
note that it is reassuring to observe that fish of a particular species have very
similar diving behavior in different oceans, conditions, and studies (K. Holland.
personal communications). Some of the most compelling arguments for the rep-
resentativeness of tracking data come from recent comparisons of acoustic and
archival records, as well as acoustic and pop-up satellite records (Boustany et ul.,
2001; Marcinek et al., 2001). These studies have revealed a good correlation be-
tween key parameters (e.g., mean swimming depth, mean water temperature)
despite the fact that data are acquired at very different sampling rates (seconds for
acoustic data, minutes for archival and pop-up tags). Comparisons of acoustic and
archival or pop-up satellite data for the same species (Atlantic bluefin tuna),
and in the same area, indicate that in some cases. but not all, the first day or two
of an acoustic track are poor indicators of the behavior of the fish (Boustany et al.,
2001). This seems most likely to be a problem if fish are caught on a hook and
line, and suggests that in some cases a recovery period is required (Block et al.,
1992). However, it is clear that individual fish have distinctly different abilities
to recover from the tagging events and not all fish are equally affected by the
experience.
With this caution in interpretation of short acoustic tracking records, it is in-
teresting to note that for most of the Thunnus species examined, the published
acoustic tracks provide a good record of the median depth distribution and ambi-
ent temperature preferences of the species. Acoustic data on the depth and ambient
temperature preferences of yellowfin tuna are the most extensive (approximately
60 days of records from 23 fish have been obtained). Comparing the results in the
literature with a larger data set from pop-up satellite archival tags indicates similar
information on yellowfin depth distribution (B. Block, unpublished data). Thus,
while in some cases the behaviors in the early portions of acoustic tracks are
clearly aberrant, due to the handling or the presence of the tracking vessel, in most
tracks the fish settle down and exhibit movement patterns that are typical of indi-
viduals tracked with archival and pop-up satellite archival tags (PATS) (Marcinek
et al., 2001). The great advantage of acoustic tagging is it puts the researcher in
the field close to the fish where interactions with prey species and associations
with other organisms can be noted.
III. ARCHIVAL TAGS
Following their successful use to study marine mammal movement and behav-
ior (Delong et al., 1992), archival or data storage tags were described as a “poten-
tial tagging technology” for studying tuna movement and behavior by Hunter
et al. (1986). The concept was a tag that would allow collection and storage of
data from a number of environmental sensors for a year. If this could be achieved,
it would fill in the gaps that existed between the very short-term and detailed data
collected by acoustic tracking studies and the single points of release and recap-
ture provided by conventional tagging experiments. Archival tags were seen as a
means of understanding residency and long-term variations in movement and be-
havior. Also, being fishery independent, they would provide much-needed infor-
mation of the movements of tuna into areas where there were no fisheries (and
thus where there had been no conventional tag returns).
A U.S. company, Northwest Marine Technology of Shaw Island, Washington,
completed a feasibility design for an archival tag in the mid 1980s. However, the
technology was not used on tuna until 1993 (southern bluefin tuna; Gunn et aZ.,
1994). Block et al. (1998a), inspired by the southern bluefin work, began archival
tagging Atlantic bluefin tuna in 1996. At much the same time, data storage tags
without light sensors were also first used on plaice in the North Sea (Metcalfe and
Arnold, 1997), and Tsuji et al. (1999) began archival tagging Pacific bluefin tuna
in pens and in the wild. The success of these independent studies has led to the
use of archival tags on bigeye (Boggs et al., 1999; J. Gunn and J. Hampton, per-
sonal communication; K. Schaefer, personal communication).
Archival tags are basically miniature computers, incorporating microproces-

sors, memory, and a suite of environmental and physiological sensors. They have
very low power budgets, allowing data to be collected over many years. Specifi-
cations vary among manufacturers (Klimley et al., 1994). However, the most ad-
vanced tags available as of this writing have light sensors capable of measuring
variation in moon light at depths of 100 m, l-4 megabytes of flash (nonvolatile)
RAM memory, depth sensors providing accuracy of < 1 m over a range of 1000 m,
and thermistors capable of measuring temperature to within 0.1 “C over a range of
4O”C+. They use 8- or 16-bit microprocessor technology and allow data to be
collected from 3-4 sensors every few minutes for periods of up to 5 years. The
nonvolatile memory allows data to be retrieved even after the tag’s battery has
run down.
Perhaps the most critical feature of an archival tag is the collection of data that
can be used in estimating the position of the tagged animal. Over the last 5 years,
researchers have used light, water temperature, and depth data collected by archi-
val tags in estimating position.
Estimating position from variation in light levels involves relatively simple
concepts and algorithms (Wilson et ul., 1992; Hill, 1994; Hill and Braun, 2001).
If tunas remained on the surface and did not migrate long distances in short pe-
riods, estimating their position from archival tag data would be relatively straight-
forward. Unfortunately, most tunas tend to make very rapid dives, often at sunrise
and sunset-the times most critical for estimating latitude with light-and all are
capable of rapid movement over large geographic scales. Thus, when using archi-
val tags to estimate the position of tunas we can expect systematic and random
errors resulting from equinoxes, light attenuation, water clarity, weather patterns,
precision of astronomical algorithms, clock errors, resolution of light sensor, and
behavior of the animal (Musyl et al., 2001).
Welch and Eveson (1999) and Musyl et al. (2001) estimated the accuracy of
geoposition estimates based on light data from archival tags by comparing the
known and estimated positions of tags attached at various depths to fixed oceano-
graphic moorings. They used tags from different manufacturers, and employed
a number of different analytical methods. Although there was variation in per-
formance between tags, and some methods performed better than others under
particular conditions, the scales of error in longitude and latitude estimates were
similar in the two studies. Briefly, longitude consistently varied less than latitude,
regardless of the analytical method used or the depth at which tags were moored.
The standard deviation of errors in longitude estimates using the Welch and Eve-
son (1999) method was -tO.9”, or approximately 60 km, while that of latitude
estimates was -+ 1.2”, or 130 km. Musyl et al. (2001) used a slightly different
method of presenting their data; the absolute mean errors (i.e., true position -
estimate) in longitude estimates for three methods ranged from 0.15” 2 0.12 (SD)
to 0.29” + 0.83, and in latitude estimates from 1.49” ? 2.12 to 4.36’ + 5.78.
As Welch and Eveson (1999) and Musyl et al. (2001) used tags that were
essentially stationary in both the horizontal and vertical planes, their estimates
provide minimum errors only. The only attempt to estimate the accuracy of posi-
tion estimates from data collected by tags on fish (Gunn et al., 1994) found mean
errors on the order of 1.52” [ +0.22 (SD)] in latitude and 0.54” (kO.09) in longi-
tude. However, as the fish used by Gunn et al. (1994) were held in cages less than
20 m deep, and the study was conducted in early January, when errors in latitude
are at their lowest (Hill, 1994), these estimates are again likely to be conservative
for animals in the wild.
There are few published accounts of tuna movements or migrations based on
archival tag geoposition estimates. However, experiences with large data sets col-
lected by archival tagging programs on southern bluefin (SBT; J. Gunn, unpub-
lished data), bigeye (J. Gunn and J. Hampton, unpublished data), Atlantic bluefin
(B. Block et al., 2001), and Pacific bluefin tuna (Kitagawa et al., 2000) suggest
that to get an estimate of position it is often necessary to use a combination of
light, surface water temperature, and diving behavior data. The latter two data
sources are used primarily to estimate latitude when light data do not allow accu-
rate resolution of the times of sunrise and/or sunset. In SBT, the proportion of
days in which light data can be used to estimate latitude varies throughout the
year, largely as a result of changes in diving behavior associated with their annual
migration cycle (see below). From late spring to early autumn, juvenile SBT live
on or close to the southern Australian continental shelf. During this period they
spend most of their time in the upper 100 m of the water column. In these depths,
light data are generally good enough to make estimates of longitude and latitude,
although the latter suffer from large interdaily variation (and thus presumably er-
ror) if fish consistently dive at sunrise and/or sunset. Errors in latitude estimates
are also high during the summer and winter solstices (Hill, 1994). During winter,
juvenile SBT migrate into oceanic waters where they make die1 migrations from
the surface (night) to depths over 400 m (day). Current generation archival tags,
with their highly sensitive light sensors, allow longitude to be estimated from light
data even during these times of extreme diving. However, as the most active ver-
tical migration occurs close to times of sunrise and sunset, latitude estimates are
rarely reliable. On these days, latitude is best estimated by comparing the records
of sea surface temperature collected by the archival tag external temperature sen-
sor with those provided by satellite SST data. If light data allow an estimate of
longitude, this can be used to examine the match between tag and satellite-
estimated SST to derive an estimate of latitude (Smith and Goodman, 1986).
5. ADVANCES IN TAGGING OFTuN,\S 181
Although it is possible to derive an estimate of position for most days using a

combination of light, environmental, and behavioral data, objective measurement
of the errors or reliability of these estimates is very difficult. For example. over
the course of a month, geoposition estimates based on light often show move-
ments that are simply impossible-either because they have tish “swimming”
across land, or they involve movements of many hundreds of miles over 24-h
periods. It is not always obvious from the light curves why one estimate is likely
to be correct while another may be spurious.
By combining light and SST data one can objectively exclude position esti-
mates on land. However, it is often more difficult to exclude positions in the ocean.
For example, when fish are close to a large-scale eddy, or are within extensive
areas of isothermal water (such as in the equatorial regions of most of the world’s
oceans), there will be a number of equally plausible latitudes for a given SST.
Several suggestions have been made on how to “objectively reject” unlikely
or spurious position estimates. Among these are:
l Limiting daily movement to a sensible maximum distance, perhaps based
on the maximum daily movements observed in tracked fish. This may be
satisfactory for fish not actively migrating. However, as we describe below.
bluefin tunas can move significant distances in one day when making di-
rected migrations.
l Limiting analysis of position to days where diving behavior at the times of
sunrise and sunset do not involve vertical movements over a defined limit.
l Using trend analysis, statistically remove outliers further than a set deviation
from a trend line in a series of position estimates. This approach is based on
the assumption that fish are unlikely to make random movements of scales
greater than some arbitrary threshold.
Whatever the approach, showing both the raw and smoothed or reduced data
is advisable, at least until more rigorous approaches have been developed to esti-
mate error of position estimates.
B. Archival Tagging of Tunas
1. SOUTHERN BLUEFIN
The first tuna to be archival tagged were southern bluetin. The species has a
wide and continuous distribution across the southern oceans of the world-from
the southwest Atlantic to the southeastern Pacific, and one known spawning area
south of Java. It has been heavily fished by Japan and Australia for over 40 years
(Caton, 1991) and the estimated parental biomass in 1998 was less than 12% of
that in 1960, and considered to be at historically low levels (Anonymous, 1998).
Despite the heavy exploitation over many decades. little is known about the spe-
cies’ spatial dynamics. Recent contractions in the sir,e and number of fishing
grounds have prompted debate over whether there has been a significant contrac-
tion in the geographic distribution of the stock, or simply a shift in the operations
of fisheries targeting the species.
Much of what was known about SBT migration derives from extensive con-
ventional tagging programs over the last 40 years. Since the 1960s over 132,000
SBT have been tagged and approximately 20,000 recaptured (Polacheck et al.,
1998). From conventional tagging data, catch records, anecdotal accounts of fish-
ermen, and, we suspect, in part also the imagination of fisheries scientists, a hy-
pothetical model of the migration of juvenile SBT was developed in the 1960s
(Hynd, 1969) and later refined by Murphy and Majkowski (1981). The weakness
of the SBT conventional tagging data set, as with many conventional tagging ex-
periments, is that the vast majority of tags have been released in a few locations-
mostly along the southern and eastern coastlines of Australia-and all of the re-
captures have been made in locations where commercial fisheries operate. Thus,
after 20,000 recaptures we know a great deal about the extent of mixing among
Australian fisheries and, for fleets where reporting rates allow, between these and
high seas fisheries. However, little is known of the residence times of fish in the
different locations, whether a significant proportion of the populations spends
time away from areas targeted by commercial fisheries, or how and when the fish
moved between the points of release and recapture. Without these critical inputs,
the models we have developed of SBT movement are seriously flawed.
To address the inadequacies in our understanding of migrations and short-term
movements of S.B.T. within the Great Australian Bight (GAB), the Common-
wealth Scientific and Industrial Research Organization (CSIRO) in Australia be-
gan to tag juvenile SBT with archival tags in 1993 (Gunn et al., 1994). Five hun-
dred and fifteen tags have been released, and 100 reported recaptured after times
at liberty ranging from 10 to 1500 days. The tags have now collected over
15,000 days of data, which have challenged many of the previous views of the
movements of juvenile SBT and provided a wealth of information on their behav-
ior and physiology (Gunn et al., 2001). We now know these fish make annual,
cyclic migrations over ocean-basin scales. Summer is spent in the warm continen-
tal shelf waters of the GAB, while in winter they range widely over the oceanic
waters of the southern Indian, Atlantic, Southern, and southwestern Pacific
oceans. We have used the archival tag data to define residence times in the summer
and winter feeding grounds and to examine the routes taken by fish as they migrate
between these grounds. The data have also provided a unique insight into the
behavior of fish in their different feeding grounds and as they migrate.
The volumes of data collected by archival tags provide an immediate challenge
of how best to summarize the complex behavior of individual fish, while drawing
out similarities across age classes, or groups of fish tagged at the same time. To
illustrate the nature and extent of the data collected, we describe below the move-
ments and behavior of one 3-year-old SBT between its release on 24 January 1998
and recapture 14 months later. For the time-at-liberty, we have a record of the
animal’s depth, its visceral temperature, the ambient water temperature, and the
ambient light level, every 4 min. The light, depth, and water temperature data
allow us to estimate the animal’s position for most of the time at liberty (Welch
and Eveson, 1999; Hill, 1994; Musyl et al., 2001). Ambient temperature and depth
data allow us to examine habitat preferences over daily, lunar, and seasonal time
scales, and the visceral temperature provides a record of whether and when the
fish has eaten each day (Gunn et al., 2001).
a. A Year in the Life ufa 3-Year-Old SBI: SBT 98-007 was 100 cm fork length
and approximately 22 kg when it was caught by pole and line on the continental
shelf edge of the Great Australian Bight (Lat. 33”17’S, Long. 131”26’E) on
24 January 1998. Within a few seconds of taking the live bait, the fish was lying
on a tagging cradle having a Wildlife Computers Mk 7 archival tag surgically
implanted into its body cavity, approximately 10 cm anterior to the anal vent. The
surgery took 1 min and after a suture to close the wound, the fish was released
back into the school from which it came. Twenty other fish from the same school
were tagged within an hour, and all were released back into their school.
Immediately after release, 98-007 dived to 30 m and for the next couple of
hours moved between this depth and the surface (Figure 3A). At sunset, it made a
brief dive to over 120 m-below the mixed layer-and returned immediately to
the surface. Shortly afterward, however, it returned to 120 m and as the night
proceeded, gradually ascended and then descended, presumably in association
with the vertical migration of the scattering layer. At sunrise, the fish made an-
other short dive to 110 m and returned to the surface. These short, “spike” dives
occurred almost every day throughout its 15 months at liberty, at exactly the same
time relative to sunrise and sunset, whether the fish was on the continental shelf
or in the open ocean. Spike dives are a common feature to all SBT archival tag
data sets. Why fish would undertake short vertical migrations almost every day at
sunrise and sunset is unknown. Possible explanations include locating the mixed
layer (as seems to have been the case in 98-007); surveying prey fields at times
when prey are silhouetted rather than camouflaged against the background; sur-
veying the geomagnetic field on a regular basis as a means of geolocating; and
surveying thermal/physical structure of the water column. Whatever the reason, it
is clear that the behavior of SBT is precisely linked to variation in light levels.
Sunrise and sunset are times when light is changing most rapidly, so the ability of
SBT to synchronize ascent and descent to within a minute or two each day sug-
gests they are very sensitive to these changes. As spike dives have been reported
(or are obvious in figures included in publications) for a wide range of pelagic
animals [e.g., blue shark (Carey and Scharold, 1990), swordfish (Carey and Ro-
bison, 1981), and yellowfin tuna (Block et al., 1997)], it seems that the motivation
for this behavior is common to many animals living in the open ocean.
A
5;
e
2
2
Longitude
B 9O”E 105”E 12O”E I35’E
15”s
30”s
45”s
C
SBT 98-007’s diving patterns (frequency of ascents/descents, diving depth

range, die1 variation) on the first day at liberty were very similar to those for the
rest of the time it spent in the Great Australian Bight. From this we could conclude
the stress of tagging did not to adversely affect the fish’s behavior. However, it is
interesting that although diving behavior seemed “normal,” the fish either did not
eat, or took only very small meals, for the first 29 days at liberty (Figure 4A).
During this period, the lack of feeding activity can be identified by the tempera-
ture differential between ambient and the viscera remaining more-or-less stable at
l.6-2°C.
Going without food for periods of weeks to a month following tagging is com-
mon among the 100 SBT recaptured after archival tagging, and suggests that the
fish take a significant time to fully recover from the stress of handling and surgery.
In some fish, diving behavior during the first 2-4 days also appears abnormal with
ascent/descent rates and intervals between dives during the first few days being
much higher that normal, and indicative of frenetic activity.
As we discussed above, a major uncertainty in the interpretation of ultrasonic
tracking data is whether the behavior observed is truly “normal.” As tracks rarely
last more than 2 days, the concern is that the stress of handling and attachment of
the tag may cause abnormal behavior. The long-term nature of archival tag records
provides a yardstick by which to measure “normal” behavior. Our data suggest
that the stress of handling can have a range of expressions in the diving and feed-
ing behavior of SBT and that these should at least be acknowledged and looked
for when analyzing tracking behavior. However, we offer one caveat -as implan-
tation of archival tags into SBT involves surgery, extrapolation of our observa-
tions to tracking studies where tags are attached externally is problematic.
On the 5 March. 98-007 took its first substantial meal (as indicated by the
+S”C differential in Figure 4B). Based on the relative magnitude of temperature
differentials. which are closely related to the amount of food consumed (Gunn
et al., ZOOI), the size of meals increased in the weeks following this first meal.
Between 5 and 3 I March, when the fish left the GAB, the fish fed every day.
While in the GAB (Figure 2). 98-007 spent the majority of its time on the
continental shelf in depths less than 100 m (Figure 5A), in ambient water tem-
peratures of 18 to 2 lo C (Figure SB). On the shelf, the fish spent a high proportion
of the daylight hours in the upper few meters of the water column, and from time
Fig. 2. (A) Fine-scale movements of SBT 98-007 between 24 January and 1 May 199X deter-
mined from light and SST data collected by an archival tag. The movements along the eastern marytn
of the Great Australian Bight are overlaid on an SST image taken 20 May 1998. (B) Movements of
SBT 98-007 between 24 January 1998 and 3 March 1999 determined from light and SST data collected
by an archival tag. (C) Composite SeaWiFs ocean color satellite image for the Indian and Southern
oceans for the first week of October 199%. rhowinp the area in which 98-007 had foraped during
September and October.
A GMT Time
6
0
50
100
150
I I
200' c 10
0
0
100
200
300
400
500
0:OO 12ao ofm 1290 0:OO

D - 35
"lu~aplh'~ -
E
5
08
Fig. 3. Archival tag ambient water temperature PC), visceral temperature (“C), and depth (m)
data for SBT 98-007. (A) The first 24 h post release in the GAB. (B) Basking in the GAB on a summer
afternoon (local time is GMT + 10.5 h) in the upper water column, and showing progressive warming
of the water and associated warming of the viscera. (C) Deep diving and die1 vertical migrations. Note
the increases in visceral temperature indicating feeding in the early morning. (D) Capture by purse
seine at around 2300 GMT (0830 local time), followed by the transfer into a cage limiting maximum
diving to leas than 20 m. Dark bars indicate night.
5. ADVANCES IN TAGGING OF TUi%AS 187
GMT Time
6:00 6:00 6:00 6:00 6:00 6:00
Fig. 4. The differential between visceral and ambient water temperatures recorded by archival
tags over S-day periods provides a means of tracking feeding activity. (A) Constant differential of
approximately 2°C indicates no feeding. (B) Minor peak on first day indicates the first significant
intake of food by SBT 98-007. followed by a series of small feeds in the next 4 days. (C) Large
differential (up to 9°C) indicates significant food intake each day. * indicate feeding events.
to time the data indicate “rippling” or basking behavior. When rippling, individu-
als swim in the upper 1-3 m of the water column (Figure 3B), rolling from side
to side thereby exposing their silver underbellies to the sunshine. The behavior is
commonly observed by fishermen and aerial spotters on days when air tempera-
tures are high (>3O”C). The archival tag data show that extended periods on the
surface are correlated with increased ambient temperatures as high levels of solar
insolation warm the surface layers of the GAB. Increases in ambient temperature
in turn result in significant warming of the viscera (and presumably the rest ofthe
b
Temperature
C
5. ADVANCES IN TAGGING OF; TCiN 4s 189
body) over periods of many hours. Although this behavior has not been reported
for other species of tunas, it is analogous to the behavior that sees many tunas
using warm core eddies or the mixed layer as thermal refugia while making for-
aging excursions into colder water. Maintenance of elevated temperatures should
increase aerobic performance (Dickson, 1995) and speed digestion of food (Carey
rt ~1.. 1984; Stevens and McLeese. 1984). We know that 3-year-old SBT accrue
80% of their annual growth while in the GAB over the summer months (Leigh
and Hearn, 2000) and thus it seems likely that the energy derived from heating
associated with long periods of rippling and surface schooling could contribute
significantly toward increasing the energy available for growth during this period.
SBT 98-007 migrated out of the eastern GAB in late March 1998 (Figure 2A),
and moved slowly in a southeasterly direction along the continental shelf. At this
time of year, a narrow shelf-break current jet flows southeast from the GAB on
the outside the continental shelf in this area, and it appears the fish followed this
warm water as it flowed out of the GAB. Although the jet pushes as far as southern
Tasmania during winter, 98-007 moved only 200-300 miles southeast of the GAB
and remained in an area west of the Bass Strait for 3 months. This area experiences
seasonal upwelling during late summer and it seems likely that the fish remained
in this area to take advantage of higher productivity associated with the upwelling.
Occasional but regular dives to 300600 m indicate that the fish remained in
ocean waters or close to the continental shelf break throughout autumn. However,
it was predominantly surface oriented, spending over 75% of its time in the upper
50 m of the water column. Ambient temperature and depth data from the tag show
that the fish frequently moved across strong thermal gradients (Figure 6) indica-
tive of movement in and out of the warm front. Associations with fronts and eddies
are common in most archival data sets and it appears that SBT use warm core
eddies or warm currents as thermal refuges while taking advantage of increased
productivity often associated with frontal systems (Franks, 1992). SBT 98-007 fed
on 46 of the 80 days it spent in the area west of Bass Strait during autumn.
In July, 98-007 moved further offshore into the Southern Ocean where it re-
mained for almost a month. In early August it began swimming steadily westward.
and continued to do so for 2 months. By late September it had reached 9O”E and
covered a straight-line distance of 7700 km in 50 days (Figure 7). This equates to
an average swimming speed over the ground of 6.4 km per hour, or 1.8 m pet
second. As the archival data indicate significant vertical movement and we pre-
Fig. 5. Frequency distrihutiona f.or (A) depth and (B) ambient water temperature for SBT WW7
in the GAB during 1998, in the western Has Strait, while migrating to and from the GAB, in the
Indian Ocean. and in the GAB during the \ummer of 1999 heforc being caught. (C) Depth frequency
distributions for full moon and new moon periods while SBT 98.007 was in the Indian Ocean feeding
prounda.
A GMT Time
20:O0 8:00 2O:OQ 8:oo 20:Oo
0 30
Temperature (“C)
B
10 15 20 25
1
300 *
350
Fig. 6. (A) Archival tag records of depth and ambient and visceral temperature showing a
2-day period in the western Bass Strait area, during which the tish moved back and forth across a 2°C
temperature front. (B) Temperature and depth data for the period shown in A indicating the two dif-
ferent water masses in which the fish was swimming. along with the mixed water between.
sume the fish was also making tine-scale horizontal movements during this time,
the true swimming speed through the water was likely to have been much higher.
On the outward migration the fish also swam directly against the west wind drift,
which at that time of year is at its strongest in the “roaring 40s.” While migrating,
feeding occurred on 36 of the 50 days, and although it spent 30% of the time in
the upper 10 m, a significantly higher proportion of the time was spent at depths
greater than 100 m than had been the case in the GAB or Bass Strait. There was
no obvious reduction in the oscillatory diving behavior during the migration, nor
a bimodal distribution of depth such as that seen in actively migrating yellowfin
(Holland et al., 1990). As the fish migrated across the Southern Ocean and into
the Indian Ocean, it moved progressively into colder water, and by the time it
reached its western-most position at 90”E, surface water temperatures were 1 l-
13”C-up to 10°C colder than during the summer season in the GAB (Figure 5B).
In the Indian Ocean, 98-007 began daily die1 vertical migrations, characterized
5. ADVANCES IN TAGGING OF TUNAS
Longitde
60 75 90 105 120 135 150
I I I I I
OW1198
24m2m -
1wo4lga -
o4mm -
d 24407/98 -
8 12mm -
01111198 -
21/12m -
oQNJ2m -
31/03m
Fig. 7. Longitude estimates derived from an archival tag on SBT 98-007, showing the two periods
during which the fish was in the eastern G4B and western Bass Strait region (longitudes 130-IMoE),
and the two very rapid migration& between these areas and the central Indian Ocean. Estimates were
made for 90% of the days at liberty.
by long periods in the upper 40 m during the night and gradual descents starting
at sunrise down to 200-400 m, followed by gradual ascents finishing at sunset
(Figure 3C). There was also a clear lunar cycle in the depth preferences at night,
with the fish being deepest during the full moon and a few days following, and
shallowest around the new moon (Figure 5C).
The vertical migration suggests a close association with the scattering layer,
very similar to that described for bigeye tuna (Dagorn et al., 2000; Holland et ul.,
1990). The area in which 98-007 foraged was to the east of St. Paul and Amster-
dam islands, on the northern edge of the subtropical convergence zone. In this
area a very deep mixed layer (temperatures on the surface were the same as those
at 300 m) allowed the fish to forage to considerable depths without having to move
into cold, subantarctic water. Productivity in the area, as indicated by NOAA Sea-
viewing Wide Field-of-view Sensor (SeaWiFs) data, was relatively high, and sig-
nificantly higher than that in the GAB at the same time.
The predominant food in the diet of SBT caught in the Indian Ocean is omas-
trophid squid (CSIRO, unpublished data), which are known to undertake large
diurnal vertical migrations, also in association with the scattering layer (Naka-
mura, 1993). Nakamura ( 1993) found that mature female omastrophids migrate to
depths in excess of 600 m each day, with descent dives starting around 1 h before
sunrise and ascents around sunset. It seems very likely that the vertical migrations
of 98-007 were in response to the squid movement. Visceral temperature data
from the tag indicate the fish began digesting a meal shortly after beginning its
descent, and small secondary peaks early in the morning were coincident with the
ascent dive (Figure 3C). Although we cannot tell from these data whether the fish
continued to feed while at depth during the day, the presence of two modes sug-
gests most feeding occurred at these times, when the squid were actively moving
through the depth range in which the fish was foraging.
After less than 2 months in the central Indian Ocean, 98-007 began a return
migration towards the GAB. It returned on much the same route it had taken on
the way out (Figure 2B), and the return journey was again very fast, taking on the
order of 60 days (Figure 7). On 4 January 1999 the tish revisited the shelf break
location it had been tagged at almost 12 months before. Once back in the GAB,
98-007 switched back to the behavioral patterns and habitat preferences exhibited
the previous summer (Figures 5A and 5B).
In the first 12 months at liberty, 98-007 covered in excess of 18,000 km in
straight-line migrations; changed habitats, diving behavior, and dietary prefer-
ences; and managed to avoid capture in the extensive Japanese, Korean, and Tai-
wanese high seas long-line fisheries that operate in the southeast Indian Ocean
during the winter-spring period. From the archival tag data we were able to esti-
mate residence times in the different feeding grounds and determine what propor-
tion of the time it had been foraging or migrating in fishing grounds.
Early in the morning of 18 February, the fish was caught by the purse seiner
FV Kathy BJ while swimming in a large school off the continental shelf in the
eastern GAB. The tag data show the dramatic change in diving behavior following
the fish’s transfer into a cage in which it was towed back to Port Lincoln on the
coast of South Australia. In Port Lincoln, the fish was fattened for 6 months before
being harvested for the Japanese sashimi market. Over these 6 months we see in
the archival tag record the daily feeding cycles of the aquaculture operators (see
Gunn et al., 2001).
2. ATLANTIC BLUEFIN
Atlantic bluefin are another tuna species for which we have inadequate under-
standing of movement patterns, where and when they breed, or how populations
are structured despite over 2000 years of exploitation (Block et al., 1998a). Like
southern bluefin, stocks of Atlantic bluefin tuna are now considered overexploited
(National Research Council, 1994). They are managed by the International Com-
mission for the Conservation of Atlantic Tunas (ICCAT), and stock assessments
currently consider the Atlantic bluefin tuna as two separate populations with lim-
ited mixing and distinct breeding grounds. One stock is proposed to reside in the
west Atlantic with a spawning ground in the Gulf of Mexico; another stock is
proposed to exist in the east Atlantic with a spawning ground in the Mediterranean
Sea (National Research Council, 1994). Importantly, conventional tag data have
demonstrated that all size classes of Atlantic bluefin are capable of making trans-
Atlantic crossings in short durations (National Research Council, 1994); however,
there is little information in the conventional tagging data with which to define
stock boundaries. To learn more about the biology, migrations, and stock structure
5. ADVANCES IN TAGGING OF TUN 4S 193
of bluefin tuna, an archival tagging program was initiated in the west Atlantic in
1996 (Block et nl., 1998a,b, 2OOla,b).
From 1996 to 1999,279 implantable archival tags were deployed in the west-
ern Atlantic on medium and giant bluefin tuna, Thunnus thynnus thynnus (Block
et al., 1998a,b). More recently, archival tags have been deployed in the eastern
Atlantic in juvenile bluefin tuna (ICCAT, 2000). To April 2001, 45 recaptures
(16%) from the west Atlantic releases have been reported. The data provide excit-
ing new insights into the seasonal movements, trans-Atlantic movement patterns,
depth preferences, thermoregulatory biology, feeding habits, and breeding behav-
iors of the species. Perhaps not surprisingly given their close genetic relationship
(Collette, Reeb, and Block, this volume), there are many similarities between the
data collected on Atlantic bluefin and those described above for southern
bluefin tuna.
All the archival tags deployed on Atlantic bluefin have been released in the
west Atlantic, on fish caught by rod and reel in the winter sport fishery that oper-
ates on the U.S. east coast near Cape Hatteras and Cape Lookout, North Carolina
(35”N, 7S”W). The implantable archival tagged fish ranged in size from 170 to
254 cm CFL (curved fork length), and at this size fish are considered to be either
western adolescents (7 years of age) or western breeders (S-t), based on the
ICCAT model of length to age transformations (Turner and Restrepo, 1994).
Although the data on the movement of each fish while at liberty are fishery
independent, the recapture locations of archival tags reflect the current distribution
of the known bluefin tuna fishery-from the Gulf of Mexico throughout the
northwestern Atlantic, eastern Atlantic, and the Mediterranean Sea. The times at
liberty for tags returned to date range from 0.2 to 3.6 years. Over 14,700 days of
data on bluefin tuna biology in the western Atlantic have been collected, providing
information on the activities of the fish on daily as well as seasonal time scales.
N. Diving Behavior-Depth trnd Thermal Habitat Preferences. As we have

seen in juvenile southern bluefin tuna, the archival tag data demonstrated a broad
repertoire of vertical movements in adolescent and adult Atlantic bluefin. Despite
the variety and complexity of some of the diving records, however, the general
patterns of vertical movement were common throughout our archival tag data sets.
and they varied in similar ways on a seasonal basis.
With data being collected every 2 min for months to years, we have used
archival tags to examine Atlantic bluefin diving behavior and thermal and depth
habitat preferences on daily, seasonal, yearly, and multiyear scales (Block et (11..
2001). The problem rapidly becomes one of how to display and summarize the
extensive data sets produced by archival tags. Figure 8A shows the maximum
depth and sea surface temperature for an Atlantic bluefin tagged in 1999 (2 18 cm
curved fork length, CFL). A depth record from a smaller Atlantic bluefin ( 193 cm)
archival tagged in 1997 ih shown in Figure 8B. Both fish display characteristic
250 -.
E
g 500~-
B
750 --
492
0 60 120 180 240 300 360 420 430 540 600 660
Day
B
5. ADVANCES IN TAGGING OF TIINAS 195
behaviors observed in many of the archival recaptures. While in the western At-
lantic, diving behavior varies seasonally in response to changes in location and
can be divided into an inshore North American continental shelf residency period
(winter and summer) and an offshore pattern exhibited in the spring and early
summer while fish are either along the Gulf Stream frontal zone or in warmer
waters near Bermuda or north of the Bahamas. Bluefin archival tagged on the
Carolina shelf region typically display an on-shelf shallow period in the winter,
followed in the spring by an offshore deep-diving period reflecting a change in
feeding behavior (Figures 8, 9A, and 9D). During the on-shelf period, dives are
often shallow and brief, and water temperatures are warm (18 -23” C). During the
offshore period the bluefin make deeper dives-occasionally to depths as great as
700-1000 m (Figure 8A). Once back on the shelf in the summer and early fall,
the Atlantic bluefin are primarily occupying the upper 200-300 m of the water
column limited in depth by the continental shelf.
Figure 9 shows the typical behaviors of bluefin tuna during the year in more
detail. The archival tagged Atlantic bluefin often remained in the vicinity of the
Carolina coast for periods of 30-90 days after release. In several cases, data from
the tags indicate that the period of residency ends on the same day or within a few
days of each other in the winter or early spring, as the bluefin migrate offshore.
While in the shallow Carolina region, the continental shelf limits vertical excur-
sions. Once the bluefin leave Carolina there are several patterns often observed.
Some fish move north immediately and encounter cooler waters as they enter the
Labrador current north of the Gulf Stream. Surface waters are often cooler (S-
10°C) than the waters at depth (inversions) at this time of year, and bluefin re-
spond by swimming in the warmer deeper waters (Figure 9B). The tagged tish
swim for long periods-in some cases weeks-in inversions and show a prefer-
Fig. 8. (A) Sea surface temperature (dots) and maximum daily depth (solid line) for a bluefin
tuna (229 cm CFL). The bluefin remained in the west Atlantic for the duration of the tag mission. The
maximum daily depth shows the deepest depth reached by the bluetin on a daily basis and provides a
view of the maximum diving patterns. Upon release off the Carolina coast the bluetin was limited in
vertical excursions by the continental shelf. A warm eddy from the Gulf Stream was situated in the
region the fish was tagged in and provided warm 1g-20°C waters. Once off the shelf and in the Gulf
Stream in March, the bluefin made occasional deep dives throughout the late winter. By early spring
the fish had moved considerably north and was moving away from the frontal boundary of the Gulf
Stream and into cold northern waters. Summer was spent feeding on the shelf. The second season the
fish moved offshore in the late fall and moved south into the warmer waters to the east of the Carolinas.
The tish did not revisit the Carolina coastal province. (B) Monthly depth histograms compiled from
archival data for bluefin tuna WC-019. This tish was a 193-cm (CFL) individual tagged on 7 March
1997. This fish displayed western residency in its track. which was characterized by shelf behavior in
the winter in Carolina, the late \ummer In New England. and once again in the second winter off
Carolina.
ii 36%
30:
26 ';;
20, 0
15
IO
6
0
~xn- 36
30
25
20
15
10
6
I6202428 6 12 18
Tern perrture (“C) Time of day (hrs)
Fig. 9. Four days from archival tagged bluefin tuna at different times of year displaying the typi-
cal seasonal cycle. For each day a profile of depth and ambient temperature (left panel, closed circles)
has been obtained from the data on the archival tag and is displayed. In the right-hand panel the 2-min
records from archival tags are displayed with depth as black; body temperature, red; water temperature.
green; and light in the first right-hand panel as black circles. (A) A bluefin off of Cape Hatteras, North
Carolina. (B) A bluefin encountering an inversion with cooler surface waters often swims where the
water is warmest, which is usually at depth. In this case the fish shows a preference for 100 m where
the water temperature is 13%14°C. Surface waters are S-6°C. (C) In New England, bluefin often dive
to the shelf bottom hut surface at regular intervals. (D) Offshore of the Carolinas in early winter,
bluefin often display a diurnal vertical migratory pattern characteristic of feeding on the scattering
layer organisms. All times are U.S. Eastern Standard Time.
5. ADVANCES IN TAGGING OF Tc!r\iAS 197
ence for the warmer water. often at IOO- to 200-m depths (Figure 9B). Tempera-
ture-depth profiles of the water column obtained by rapid dives called “Tuna
bathythermographs” (TBTs) reveal the structure of the water column (Figures 9
and 1 1B). Other fish move due east or southeast along the frontal zones of the
Gulf Stream or into the Gulf Stream waters south of the Carolinas. Fish moving
along the edges often work the warm core rings. In summer and early fall, the
archival tag data indicate that the bluefin of the year classes tagged are most often
on the continental shelf off New England and Canada (Figure SC). During this
period, bluefin commonly dive at dawn and dusk, and spend the morning hours
feeding and afternoon hours basking near the surface. Feeding is often associated
with the periodic reductions in peritoneal temperatures and concomitant warming
that can exceed 32°C. Body temperature often approaches 30°C during the bask-
ing periods. Periodically in the spring and the early winter months when offshore,
most often while in the Gulf Stream, the bluefin display behaviors that include
long periods of diurnal vertical migratory diving (Figure 9D) similar to that re-
ported for swordfish (Carey and Kobison, 1981) and those seen in bigeye (Holland
et ul., 1990, 1992) and southern bluefin tuna (this chapter). We hypothesize that
in all these species the diurnal periodicity in deep-diving behavior is associated
with feeding on squid, crustaceans, or octopus within the deep scattering layer. In
support of this hypothesis, we have often found squid, deep-water octopus, and
even a nautilus in the stomachs of fish (B. Block, unpublished data).
A demonstration of the endothermic capacity of Atlantic bluefin is displayed
during die1 vertical migrations when Atlantic bluefin often keep their peritoneal
temperatures elevated throughout dives, which last for many hours. The bluefin
display significant seasonal variation in the thermal excess maintained between
ambient water and visceral cavity temperature, and there is considerable evidence
to support the contention that Atlantic bluefin tuna are the most endothermic te-
leost in the ocean (Carey et cl/., 197 I ). Our data demonstrate Atlantic bluefin fre-
quent waters between 2.8 and 29.O”C (Figures 8, 9, 12; Block, unpublished data).
and throughout this range peritoneal temperatures remain significantly above am-
bient. In warm Gulf Stream waters (20-26°C) peritoneal temperatures were 3-
6°C above ambient, and relatively constant with a range in mean peritoneal tem-
peratures of 25.2-266°C. In these warm waters, deep dives to 300-1000 m re-
sulted in very small drops in peritoneal temperatures. In contrast, when in coolet
shelf or offshore oceanic waters, Atlantic bluefin maintained a differential of 1O-
15°C between peritoneal and ambient temperatures. In some individual bluefin.
but not all, when challenged by extremely cold surface waters (S-l 0°C) for pro-
longed durations, the core temperature has dropped significantly. We hypothesize
that the bluefin may be dumping heat from the oxidative muscle and viscera to the
cardiac system to protect the heart over long durations from prolonged cold. The
lowest peritoneal temperature recorded is 13°C. In addition, in some but not all
bluefin. when deep dives were made in cool surface waters (SST 5 - 10°C) for
prolonged periods, the fish often returned to the surface repeatedly. A similar pat-
tern has been reported in bigeye tuna, and is indicative of a thermal limitation and
behavioral thermoregulatory responses (Holland et al., 1992). Thus, while bluefin
show a remarkable ability to maintain a thermal excess above ambient, there are
occasions in cold waters when a physiological process is clearly limiting the blue-
fin’s dive time.
b. Seasonal Movements. Archival tag data indicate that bluefin tuna tagged in
the west Atlantic display at least three distinct types of behaviors: (1) western
residency with no visitation to spawning areas, (2) western residency with Gulf of
Mexico breeding, and (3) trans-Atlantic migrations to the east Atlantic or Medi-
terranean Sea (Block et al., 2001a,b). Archival-tagged western bluefin tuna have
been located in both known breeding areas, the Gulf of Mexico and the Mediter-
ranean Sea, during the peak of breeding season. The movements of a 1997 tagged
Atlantic bluefin (NMT 153) are shown over 3 years in Figure 10. This record is
typical of western recovered archival-tagged Atlantic bluefin tuna and shows 3
consecutive years of western residency. This fish was among the youngest fish
tagged and the behavior most likely represents an adolescent feeding route.
100
g 150
.: 200
z
250
90 80 70 60 50 40
Longitude (Degrees)
Fig. 10. Three years (19961999) in the life of a bluefin tuna (NMT 153) showing three seasons
of western residency with no visitation to the Gulf of Mexico. The general pattern is Carolina waters
in the winter, offshore in the spring, New England in the summer, and back to Carolina in the fall.
Many of the 1997 archival returns show this pattern of movement. Larger fish tagged in 1999 displayed
eastern migrations. Bathymetry and sea surface water temperature are used to augment the light data
set to determine latitude (not shown).
5. ADVANCES IN TAGGING OF ‘TUNAS 199
All of the archival tracks begin in the winter (Julian date I-90) at the longitude
of the release point, off the coast of the United States in the vicinity of North
Carolina (75”W), and most often proceed offshore in the spring along the path of
the Gulf Stream. Many of the tags display a similar western loop of travel with no
visitation to the Gulf of Mexico spawning ground. These fish move toward the
mid-Atlantic after tagging, sometimes crossing the 45”W meridian that forms the
stock boundary. Bluefin tuna displaying a western residency pattern move back
toward the New England and Canadian shelf in early summer (67-7O”W) and
proceed down the North American continental shelf toward the Carolinas in late
October and November. In “western loop” tracks the bluefin were often located
at the same longitude of release (75”W) a year later. Importantly, these fish show
no visitation during this year to the Gulf of Mexico spawning ground (>82”W).
External temperature data throughout the tracks do not show residency in any
waters that are considered warm enough for breeding (SSTs greater than 24°C for
extended periods of time in the spring and summer). In contrast, these tracks often
have water temperatures and bathythermograph profiles in the springtime that are
strikingly cold, characteristic of moving north after the Carolina residency period.
The remainder show movement along the frontal edges of the Gulf Stream. There
are several cases in which bluefin tuna that display western loops without Gulf of
Mexico visitation are in waters in June and July that are 23-25°C and warm
enough for breeding (Block et cd., 2001a).
Bluefin tuna that move from the Carolinas to a known breeding ground (Gulf
of Mexico or the Mediterranean) show movement patterns that raise many new
questions about the biology of Atlantic bluefin tuna. Bluefin are capable of rapidly
moving to the Gulf of Mexico (for example) from oceanic feeding regions thou-
sands of nautical miles away from the breeding grounds in a very short period of
time. The records are marked by a striking temperature pattern that reveals resi-
dency in warm waters during the May, June, or July period (Block et ul., 2001 a).
Temperatures during this period range from 25 to 29” C, as expected for breeding
in this species. Diving behavior for the bluefin at the breeding grounds is consid-
erably distinct from the repertoire of behavior observed in feeding bluefin tuna.
The most striking aspect of the breeding ground visitation is the short duration
(often less than a month). This suggests that in giant bluefm, spawning durations
are perhaps much shorter than previously thought.
To date a total of 15 archival tags have been reported as having been recap-
tured (fourteen with physical evidence such as the conventional green tag) in the
eastern Atlantic or Mediterranean Sea yet only 7 archival tags have been physi-
cally returned for analysis. Six fish have been reported near the straits of Sicily, or
south of Malta, in May and June. ‘Three from the mid-Atlantic, one a few degrees
south of Iceland, three near the Straits of Gibraltar, and three north of the Canary
Islands. The recovered archival tags in the eastern Atlantic and Mediterranean Sea
document trans-Atlantic crossing in short durations (50 days; Block et al., 200 la).
Importantly these tags indicate that mature bluefin tuna in the west are capable of
moving quickly into the eastern Atlantic and Mediterranean Sea (Block et al.,
2001a). Several fish show residency in the Mediterranean during the peak spawn-
ing time, suggestive that they may have fed in the west for 1 to 3 years prior to
returning to the Mediterranean to breed. Many of these fish show long periods of
western residency followed by eastern migration, perhaps to spawn.
3. BICEYE
Three archival tagging projects have independently tagged bigeye in different
parts of the Pacific Ocean over the last 2 years-in Hawaii (R. Brill, M. Musyl,
and C. Boggs, personal communication), the eastern tropical Pacific (K. Schaefer,
personal communication), and the southwest Pacific (J. Gunn and J. Hampton,
personal communication). The data from returns are now being analyzed and will
provide invaluable information on the extent and nature of regional differences in
behavior and movement.
Bigeye pose a difficult problem for those interested in using archival tag data
to estimate geoposition. As various researchers have reported from acoustic track-
ing studies (Holland el al., 1990, 1992; Dagorn et al., 2000), bigeye undertake
significant die1 vertical migrations that begin with a descent at first light each day
(before the sun rises) and end in an ascent at around last light (often after sunset).
Thus, estimating sunrise and sunset-two critical parameters for estimating geo-
location-from archival tag light data is often impossible. Boggs et al. (1999)
successfully used the regular diving ascents and descents of archival tagged bigeye
to calculate position.
The archival tag data we have collected to date support many of the observa-
tions made by acoustic tracking studies. The data come from two 12-kg fish re-
leased in the Coral Sea and recaptured after 3 and 9 months at liberty, These show
regular die1 vertical migrations from mean depths at night of 50 m down to mean
depths of between 450 and 500 m during the day. The maximum depths recorded
by both tags were greater than the 1000-m maximum readings provided by the
tag. During the day fish were regularly swimming in water temperatures of 7-9°C
(SST was 25-27”(Z), and the lowest temperature recorded was 3S”C, at a depth
estimated from the slope of the temperature-depth relationship to be over 1500 m.
C. Summary
In summary, archival tags have been used successfully in three species of tuna
to collect over 20,000 days of data from more than 150 individual fish. This com-
pares with around 120 days of tracking data from 60 fish using acoustic tags.
From the two most comprehensive data sets, on southern bluefin and Atlantic
bluefin, we have been able to define residency for tagged fish in various habitats
as they undertake seasonal and annual migrations. The cyclic nature of these mi-
grations in both bluefin species-whereby animals were recaptured very close to
their point of release, but after making migrations of many thousands of miles-
is a striking reminder of some of the limitations of conventional tagging experi-

ments. In a conventional tagging experiment, the net movement of each fish would
have been minimal, and unless significant returns had been recorded at locations
along the migration route, the inferences made of migratory patterns incorrect. In
the case of Atlantic bluefin, archival tags have provided the first details of trans-
Atlantic movements. In SBT the tags have shown that many fish move into areas
where fisheries no longer operate-an important observation in the context of
current debate about geographic contraction of the stock.
The power of archival tag data is in the ability to link behavior and environ-
mental data over long time series and ocean-basin geographic scales. This link
cannot be made as directly as in an acoustic tracking study. However, the integra-
tion of tag-derived data (fish position, diving behavior, feeding patterns, and pref-
erences and shifts in thermal habitat) with climatological and remotely sensed
oceanographic data (e.g., SST, ocean color, ocean height) provides an unparalleled
opportunity to study and perhaps explain patterns of migration, particularly where
these are related to feeding rather than spawning. Answering some of the key
questions regarding the causal factors behind large-scale migrations and habitat
shifts should provide us with a much better basis for interpreting large-scale
changes in abundance of tunas such as those described in association with El Nino
cycles in the Pacific (Lehodey et rrl.. 1998).
Although the appeal of archival tag technology is obvious, there remain some
serious limitations to its use in some tuna species. The first is that we remain depen-
dent on fishers to return the tags for data to be collected. For Atlantic bluefin, in
more than 20% of the recaptures of tagged fish, tags have not been physically re-
turned. In southern bluefin, the recapture rates for high seaslong-line fleets are sig-
nificantly lower than expected given their catch rates on tagged cohorts. As with
conventional tag reporting rates, there are many reasons why fishers choose not to
cooperate. Regardless of the reason, low recapture and/or low reporting and return
rates seriously compromise archival tagging experiments, and it is likely that the
likelihood of success will relate to how much cooperation one is likely to get from
fleets catching the tagged fish. Interestingly, however, return rates for archival tags
are significantly higher than those for conventional tags in SBT and Atlantic bluefin
tuna, indicating either much lower shedding rates. or higher reporting.
The second major limitation of archival tags derives from the interaction be-
tween the behavior of fish and the technology. Over the 7 years archival tags have
been used on tunas, there have been problems with the reliability of every genera-
tion or model of tag used, and it is clear that tunas provide a harsh test on the
engineering skills of manufacturers and the durability of components. Failures due
to deep diving. wear and tear on tag stalks. battery reliability, extreme temperature
shifts over short periods as fish dive from tropical surface waters to great depths
where 3 -4°C temperatures occur, L,imitations of the light sensors have resulted
in lost data and compromised some of the data collected. It is also clear that geo-
location estimation from light data is going to be a problem for species (or size
classes) that make die1 migrations. We have been using cutting edge technology,
and perhaps it is too much to expect failure-free operations. However, an improve-
ment in the reliability of tags at this stage is much more important than major
advances in tag functionality.
IV. POP-UP SATELLITE TAGS
The recovery rates of conventional and archival tags for many species of tunas
and billfish are low, and likely to be fishery dependent. Thus, the concept of a tag
that could be attached to a fish for a predetermined period and then automatically
release and float up to the surface, where it would report its position, has been a
very attractive “potential tagging technology” (Hunter et al., 1986) for many
years. Throughout the 1990s satellite tracking technology proved highly success-
ful for monitoring large-scale movements of marine mammals, sea turtles, and
albatross (Papi et al., 1995; Renaud and Carpenter, 1994). For animals large
enough to carry satellite-linked data recorders (cetaceans, seals, sea turtles), sig-
nificant information on geoposition, swimming speed, diving behavior, and mi-
grations has been obtained for periods of a year or more (McConnell et al., 1992;
Martin ef al., 1993; LeBoeuf et al., 1996). Satellite telemetry has also been suc-
cessfully applied to animals that spend significant amounts of time close to the
surface, and are large enough to tow a floating satellite tag [e.g., basking sharks
(Priede, 1984), whale sharks (Stevens et al., 1998), and blue sharks (F. Carey,
unpublished data)]. However, for tunas and other oceanic vertebrates that remain
continuously submerged, these approaches are challenging to implement.
On a trial basis Gunn et al. (1995) used “pop-up radio tags” to define the
short-term movements and school fidelity of juvenile SBT. Using radio transmit-
ters housed in a buoyant tag body, and a timed galvanic release, they released a
group of tags in different schools. A plane fitted with a radio receiver was then
used to examine the pop-up location of the tags. Only a small number of tags were
detected, leaving open the question of whether fish had moved out of the search
area, or the bad weather experienced during the search period seriously attenuated
the radio signals from the floating tags. Since 1997, single-point pop-up satellite
tags and archival pop-up satellite tags have been used very successfully to study
the movement of large Atlantic bluefin tuna (Block et al., 1998b; Lutcavage et al.,
1999a), Pacific bluefin tuna (Marcinek et al., 2001), and yellowfin and albacore
tuna (B. Block, unpublished data). Our objective here is to describe the evolution
of the technology, and review the available data.
Two manufacturers-Wildlife Computers, Inc., of Seattle and Microwave Te-

lemetry, Inc.. of Maryland-produced their first generations of single-point pop-
5. ADVANCES INTAGGlNGOFTI'Y4S 203
up tags in the late 1990s. The tags were very similar in design and functionality.
They consisted of a lithium battery, microprocessor, low-power satellite transmit-
ter, and thermistor. The electronics were packaged in a carbon fiber or polyure-
thane tube, to the trailing end of which a streamlined float constructed of syntactic
foam, a micro-balloon resin composite, was attached (Block et al., 1998b). The
tags were designed to be attached externally to a fish; release at a preprogrammed
time through activation of a current to a corrosive link; float to the surface; and
then transmit continuously for a period of days to weeks to ARGOS satellites. The
ARGOS satellites serve to both uplink data and calculate an end-point location.
The tag’s final position is calculated using the Doppler shift of the transmitted
radio frequency in successive uplinks received during one pass. If the tag remains
attached to the fish for all of the time between attachment and pop-off, it provides
a fisheries-independent measure of the straight-line distance traveled from the
point of tagging (Block e6al., 1998b; Lutcavage er al., 1999a).
The original single-point tags produced by Microwave Telemetry provided an
end-point location and limited temperature data. The first tags utilized recorded
hourly temperature measurements and reported back 61 single hourly points dur-
ing deployments of l-3 days (Block et al., 1998b). The first software revision
applied to the first-generation tag permitted the tags to record hourly a single mea-
surement and compile a daily average ambient temperature based on the 24 mea-
surements. The tag logged 1500 individual ambient temperature measurements
that were summarized into 61 daily average temperatures. This limited data stor-
age capacity provided useful data on the overall ambient temperature preferences
of the fish carrying the tag but was often seen as a limitation to the early tag
design. However, the objectives of the initial deployments were to perfect the tag
design, improve the flotation collar based on transmission results, and examine
survivorship of fish carrying the tags. The preliminary studies proved immediately
successful-pop-up rates in short (3-14 days) as well as longer (60-90 days)
durations were high in their first applications on Atlantic bluefin tuna.
Short-term experiments were designed to test not only the new technology but
also the survivorship of bluefin tuna released after capture with rod and reel tech-
niques and attachment of the tag (Block et al., 1998b). Using the heaviest tackle
(60- and 90-kg line) and circle hooks, fishermen were able to keep times for capture
down to a minimum, even for the large fish. In all cases, the bluefin tuna were pulled
on board the vessel onto a vinyl wet foam pad, blindfolded, and irrigated with a sea-
water hose. Tags were carefully positioned at the base of the second dorsal tin and
almost always the hook could be removed. All of the above presumably cut down
stress of capture and handling. One hundred percent of the nine short-term tags
(< 14 days) surfaced and provided data. Long-term tags (deployed for 60 -90 days)
provided end-point data positions and archived a limited temperature data set (2.5of
28) providing information on whether the tag remained on the fish and if the fish
survived. Additional studies, conducted in the summer and fall of 1997, demon-
strated that pop-up tags could be attached to Atlantic bluefin as well asother marine
fish for long durations (blue marlin were tagged for 60-270 days; B. Block and
H. Dewar, unpublished data). Lutcavage et al. (1999a) attached tags to Atlantic
bluefin for as long as 270 days. Once the pop-up tags were attached for longer du-
rations, new concerns arose as it became extremely difficult with the use of the lim-
ited archive of temperatures to discern if the tags remained on the fish or had pre-
maturely released. This was particularly problematic in species of fish that
frequented warm waters with deep mixed layers (such as the blue marlin). The need
for a pop-up tag with increased archival capabilities as well as a pressure sensor was
apparent. Another shortcoming in the early generation of pop-up satellite tags that
was exposed by data coming in from archival tags was that they were possibly not
able to withstand the pressures exerted at the depths large bluefin can swim to-
commonly in excess of 1000 m (Block et al., 2OOla).
Pop-up satellite tag technology evolved quickly through several generations
of tags in the late 1990s. Second-generation pop-up tags constructed by Wildlife
Computers recorded temperature every 30 min and provided a continuous record
from deployment to the pop-off date. Although the basic external design was simi-
lar to the first-generation tags, several major changes improved performance. This
generation of tag was significantly lighter in water and had a weight distribution
that prevented the nose cone from rubbing into the fish’s body, a problem with
first-generation technology. The antenna was constructed of a flexible material
that has memory and was smaller than that of the first-generation tags. This re-
duced potential interaction with the body of the fish. The pop-off stainless steel
tube used for release was recessed into the nose cone of the tag, protecting the
stainless steel from interactions with the body of the fish. The float had a more
efficient surface to volume ratio maximizing buoyancy for a given mass, and a
high-density syntactic foam capable of withstanding pressures over 1500 m was
used. Five of these tags were placed on hook-and-line caught fish or harpooned
onto free-swimming giant bluefin tuna released in purse seines in 1998 off New
England, and all provided end-point positions and continuous thermal data. The
increased thermal archive was particularly useful for discerning whether the tag
had remained on a fish throughout its programmed attachment-an uncertainty
for earlier generation tags.
The most recent generation of Wildlife Computers pop-up satellite archival
tags-incorporating a fully functional archival controller board, as well as pres-
sure and light sensors-represents a major step forward in the evolution of the
technology. Increased efficiency of the satellite transmissions, resulting from al-
terations to the antenna and the use of a spectrum analyzer to tune the frequency
output of the PTT, is providing significant improvements in the volume of usable
data being transmitted per tag. This generation of tags archives data on tempera-
ture, depth, and light intensity, and if recovered, the data set that can be down-
loaded is identical in quality to those from archival tags (pressure, ambient tem-
perature, and light-based geolocation estimates based on light intensity data).
5. ADVANCES IN TAGGING OF TI’YAS 20s
Perhaps most excitingly, this tag has software that estimates local noon (required
for calculation of longitude; Figure 11C) and transmits these data together with a
selection of light data that can be used in the calculation of longitude and latitude.
The tag also provides depth-temperature profiles, sea surface temperatures. and
maximum depth readings (Figures I 1A and 1I B). Data collected on depth and
temperature preferences recorded in user set intervals (I to 2 min) are stored as
histograms and transmitted back (Figure 12). Software functions allow the user to
prioritize which data to send back.
Recent generations of the Microwave Telemetry tags also provide on-board
geolocation estimates and increased data storage capacity. Lutcavage rr [I/.
(2000b,c) report on the release of 2 1 “fully archival” Microwave Telemetry tags
on giant bluefin. The limited data shown in the second paper indicate that these
tags provide estimates of latitude and longitude, and allow the track of an indi-
vidual to be reconstructed based on daily position estimates. Using “proprietary
software written by Microwave Telemetry,” Lutcavage et ui. (2000~) report an
accuracy of 2” and I” for latitude and longitude, respectively, and cite work in
preparation (Paul Howey, Microwave Telemetry, Inc.) which allows for more ac-
curate geoposition estimates to be estimated following additional data processing.
The scientific community has benefited immensely from the collaborative ap-
proach taken by the two pop-up tag manufacturers with scientists using the tech-
nology. As a result, we have significantly advanced the capabilities of these tags
in a very short time. Work on ground-truthing or validating the data collected by
the tags has been slow, and to some extent has taken a back seat to the applications
work we discuss below. It is very exciting to get hold of a new technology, and
very tedious finding out how reliable it is. Perhaps the major challenge of the next
few years is to examine rigorously the potential of pop-up tags to accurately cal-
culate geolocation on board. We have seen in archival tags that estimating geolo-
cation from light data is potentially very difficult, even where one has all of the
data collected every 2 to 4 min over periods of months to years available for anal-
ysis. In addition, low transfer rates to ARGOS receivers (they can uplink only
32 bytes of data during each transmission) and the need to keep tags down to a
minimum size (the battery is the largest component in the tag) mean that it is
currently impossible to transmit all the data collected by pop-up tags for post-
processing and analysis of geolocation. There are additional complication-the
percentage of data recovered and the error rates in transmissions are heavily infu-
enced by weather during transmission, water temperature, and latitude. The bat-
tery life at the surface for the current generation of Wildlife Computers tags has
averaged 12.3 days in 18°C waters. and our experience suggests that 32-byte mes-
sage transmissions have at best a 20 -30% error rate over an entire data set. Future
tags will need to incorporate software that can calculate positions on board and.
to maximize the uploading of data, also be able to time transmission of data to
coincide with passes of satellites.
A
Julian Date 2000
96 105 115 126 135 14s 122
Temperature (“C)
IS 20 25 30
0
50
5 200
8 250
P
300
350
400
C
West Longitude
so 80 70 60 50
lO/lmO
10/11/00
10/21100
10/31/00
3 ll/lO/OO
P
11/20100
11/30/00
1200100
12/20/00
Users also require an objective test of the accuracy of position estimates made
by the tags. To provide these, at least in the best-case scenario of tags attached to
fixed buoys, experiments similar to those conducted for archival tags by Welch
and Eveson (1999) and Musyl et al. (2001) are currently under way. Experiments
examining the accuracy of pop-up satellite tag estimates are also being conducted
by attaching both pop-up and conventional satellite transmitters to marine mam-
mals (R. Hill and B. Block, unpublished data).
B. Application of Pop-Up Satellite Tags on Tunas
Over the last 4 years, pop-off tags have been successfully deployed on four
species of tuna (Table I). Although there is some question surrounding the ability
of small tunas to carry pop-up tags for significant time periods, the current gen-
eration of tags have been successful on tunas ranging from 18 kg (albacore) to
400 kg (giant bluefin tuna).
The technology has been used most extensively on Atlantic bluefin tuna
(Block et al., 1998b, 2001; Lutcavage et al., 1999a, 2000). These applications
started with testing of the technology and examination of attachment strategies in
1997 by Block et al. (1998b), and more recently the tags have been used for tar-
geted studies on specific biological and stock structure questions associated with
the management of the bluefin fishery in the Atlantic and Mediterranean Sea. We
are aware of approximately 300 pop-up satellite tag deployments on Atlantic blue-
fin, at various locations throughout their range, by a number of different tagging
teams. These deployments have met with varying degrees of success, and have
resulted in pop-ups after durations ranging from 3 to 365 days (Block et d.,
1998b, 2001; Lutcavage et al., 1999a. 2000b,c,d).
Block et al. (1998b, 2001. and unpublished data) have collected a compre-
hensive data set on movements of medium and giant Atlantic bluefin over the last
4 years, and have been able to compare these Doppler-based end-point positions
and archived pressure and temperature data sets with archival tag data collected
on fish released in the same areas (Boustany et al., 2001; Block et al., 2001 h).
Fig. 11. The types of data that are transmitted via ARGOS from the archived data set on a Wild-
life Computers pop-up satellite-transmitting archival tag. (A) Maximum depth (solid line). surface
temperature (black circles), and temperature at maximum depth (open circles) from an Atlantic bluefin
tuna in the Gulf of Mexico. (B) Comparison of a tuna bathythermograph (TBT) and an Expendable
bathythemmgraph (XBT) profile from a Gulf of Mexico fish. (C) An example of longitude data trans-
mitted from an Atlantic bluefin tuna released in Nantucket. Massachusetts, with a pop-up position oil
of Cape Hatteras, North Carolina. Releasr and recovery are ahown with an open circle. In addition to
these data, depth and temperature measul-cment\ obtained at a user set Interval (usually 2 min; see
Figure 12) are transmitted back. and a full ;,rchival record can he obtained if the tag is recovered..
PSAT 99-710
A Time at Depth April 6 - June 4,200O
100
80
8 70
80
_~.--__-.
ctiw 1n 00:0006:00
~nos:oo-i2:oo
0B 30 'bl2:00-18:00
p 20 ;D18:00-24:OO'
~~ ~~-~...
10
0
Depth Bins (m)
B PSAT 99-710
Time at Temperature April 6 -June 4,200O
loo
80
.E 80
70
$ 80.
3 50 H OO:OO-O6:d
5 40~ ;006:00-12:00
22 50.
zo- jm 18:00-24~00
10
01
Temperature Bins ("C)
Fig. 12. Pop-up satellite depth and temperature data compiled from a bluefin tuna in the Gulf of
Mexico. The pressure and ambient temperature data were collected for 2.min intervals for the duration
of the deployment and summarized into the bins as shown. Bluefin tuna in the Gulf of Mexico have a
wide depth range and a preference for warmer temperatures.
Table I
Deployment 01’ Pop-tip Satellite Taps on Tuna Species. 1997-2000
% successful
Tag Tag Number Duration Size data
Fish species Yeal manufacturer generation tagged (days) (kg) recovery
-
Atlantic bluefin tuna I997- 199X Microwave
Telemetrg I 4’ j--365 Xl-121 92
199x -_ 1999 Wildlife
Cumputerb 1 3X
I w--XKNi Wildlife
Computer\ .i I IO 1-365 JO-300 Y(P
Yehwtin tuna I997 Microwave
Telemetry I L!
Yellodin tuna 2ooo Wildlife
Computer7 2 I0 2 97 30-8Y 70
Pautic bluefin tuna 1999 Wildlife
Computers 2 3 14-60 20 -30 100
Pacific bluefin tuna 2000 Wildlife
Computers 3 6 I-l-60 15-25 I ooc,
Albacore tuna 2000 Wildlife
Computers I 2 7-l-2 18 50
From Block ( 199Xx unpublished data) and Marcinek er ol. (2001 J.

“Ongoing research (Block I99Xa. 2OOia) and Q reflect\ \ucce\\ of tag\ that have come up to date
They have successfully pop-up tagged fish off North Carolina in the northwest
Atlantic (125) the Gulf of Mexico (20), New England (25), and the Mediterranean
Sea (25). Many tags are still on fish and due to pop up in 2001; however, the
distribution of the single end points from fish tagged in the western Atlantic in
1997-2000 mirrors the archival data. Tags programmed for durations of 3 to
365 days, released initially in the Carolinas (n = 68) as well as New England
(n = lo), show a seasonal distribution around the western north Atlantic. Four
bluefin have crossed into the eastern Atlantic close to the 45” meridian. To date
no pop-up tagged western Atlantic bluefin tuna has been reported from the Medi-
terranean Sea. The difference between the pop-up satellite and archival data sets
(where 30% of the recovered archival tags are in the eastern Atlantic and Mediter-
ranean Sea) is most likely due to the length of time that the pop-up satellite tags
are placed on bluefin (3-365 days versus as long as 3-6 years). Archival tagged
bluefin apparently have diffused across their range whereas the pop-up tags to date
reveal primarily western Atlantic movement patterns with some crossover in the
spring period at the 45” meridian.
The pop-up end-point positions from release of some of the Atlantic bluefin
tuna tagged in the vicinity of North Carolina and New England are shown in Fig-
ure 13. From these data (tags were deployed for 60 -365 days) the seasonal move-
ments of the bluefin emerge and corroborate the archival data set. Carolina-
released bluefin show an inshore period of residency along the Carolina coast in
the winter months and an offshore one along the productive front of the Gulf
Stream in the spring, and report from several locations in the summer (New En-
gland, as well as offshore). Several of these latter fish have popped up in the
warmer waters surrounding Bermuda as well as the mid-Atlantic in the spring and
early summer (Block et al., 1998b; Block et al., 2001a). Bluefin tagged on the
Gulf of Mexico spawning grounds in spring have remained there for up to 60 days,
and several have moved outside the Gulf into the Florida Straits, the Bahamas,
and off the coast of the Carolinas (not shown in figure). The Gulf-tagged bluefin
tuna show a wide range of depth preferences and a characteristically warmer water
preference at this time of year (Figure 12). Giant bluefin tagged in New England
have migrated along the North American continental shelf in the fall and early
winter, similar to the positions observed on archival tags for this season, and have
in some cases popped up in the Carolinas. Several New England fish have popped
up in the mid-Atlantic, and one showed fidelity back to the New England region a
year later. As with archival tag data, the positional information can be overlaid on
SST and ocean color remote imagery to provide information on the movements in
relationship to oceanographic features such as fronts or regions of upwelling (Fig-
ure 14). Perhaps the most remarkable aspect of the 1997-2000 deployments in the
western Atlantic is the high recovery rate of data-90% of the tags reported po-
sition and archived data sets.
Based on successful pop-ups of 49 tags deployed between 1997 and 1999 on
Fig. 13. Distribution of some of the pop-off end points (<60 days) from bluefin tuna released in
1997 (black circles) and 2000 (white circies) from the Carolinas, and in 1998 from New England (red
circles). All tags shown are deployed for 60-180 days.
giant bluefin off New England in the northwest Atlantic Ocean, Lutcavage er ~1.
(I 999a, 2OOOb,c,d)have argued for a reconsideration of the current assumptions
about the species’ migration patterns, mixing rates, spawning areas, and stock
structure in the western Atlantic. While the majority of tags released in these stud-
ies popped up in the west Atlantic in locations similar to those reported above by
Block and colleagues, a significant percentage (30%) of the recovered releases
(n = 9) reported back from east of the 45”W parallel of longitude used as the
separator between “eastern” and “western” stocks. Lutcavage and her co-workers
indicate that these tags have reported back from the central Atlantic at times when
“western” Atlantic bluefin are known to spawn in the Gulf of Mexico. From this
she concludes that spawning may also be occurring in the mid-Atlantic. This is
obviously a very interesting hypothesis; however, further clarification is required
as in some cases the date the tag surfaced (e.g., March) and the size of the tish
tagged may not be inclusive of western breeders. Most recently (Lutcavage rt CZL.,
2000~) data from archival pop-up tags have also provided detailed information on
the tracks taken by tagged fish as they migrate out into the central Atlantic. Al-
though the data shown in this paper indicate that some individuals move as far
south as the Bahamas before joining the Gulf Steam on a northeasterly migration,
thus far no fish from this study has migrated into the Gulf of Mexico.
In corroboration of Lutcavage’s observations, both archival and pop-up satel-
lite data sets of Block et nl. ( i998a. 2001 a,b) indicate bluefin are often outside the
212 JOHN GIJNN AND BARBARA BLOCK
Fig. 14. Pop-up end points (black circles) on SeaWiFs data showing the productivity around the
Capes in the winter season. The productive waters attract menhaden, and bluefin appear to congregate
in this region to feed.
Gulf of Mexico at a time when breeding occurs. However, archival tag data sug-
gest that the length of time individual fish spend in the Gulf of Mexico breeding
ground is relatively short (as small as 2 weeks) and that fish that breed in the Gulf
of Mexico can be back in New England, the Bahamas, or the mid-Atlantic in a
very short period after visitation to the breeding ground. Clearly this is a fascinat-
ing and important area for future research. The plausible explanations for the data
collected to date by pop-up and archival tags appear to be one of the following:
(I) Eastern Atlantic spawners are on the west Atlantic side and move back to the
east to spawn (which is consistent with both data sets showing western-tagged fish
moving back to the east) (Block et al., 2001a). (2) Spawning occurs outside the
Gulf of Mexico; however, clarifying when and where is premature with single-
point pop-up tags with limited archival capabilities. (3) Atlantic bluefin do not
make annual spawning migrations. (4) The spawning period is extremely short
lived (as suggested by implantable archival data) and fish can be half an ocean
away in a short duration after spawning. With more releases of archival pop-up
tags planned over the next 2 years by both the Block and Lutcavage teams, and a
continuation of archival tag returns also expected over this period, there is likely
to be more data available to examine the latter two alternatives. Conclusive evi-
dence for the second option, however, would require the capture of larval Atlantic
bluefin in this area.
In southern bluefin tuna, large, adult fish are often caught in locations thou-
sands of miles away from the spawning grounds during the species’ extended
summer season. These fish are not believed to be spawning, and it is unknown
whether they make very quick migrations to the spawning ground, or alternatively
do not spawn every year.
C. Summary
Although in many ways we are still in the early stages of the development of
pop-up tag technology, it has quickly demonstrated that it can be a useful and
powerful tool in our quest for information on tunas and other large pelagic fishes.
Its most appealing and important feature is the capability of delivering data on
movement and behavior completely independent of fisheries and fishers. If we can
validate the accuracy of smart, on-board software currently being developed by
the two major manufacturers to calculate positions on board fish and/or to choose
data that when downloaded can allow users to calculate positions back in the labo-
ratory, then pop-up tags have the potential to answer many of the most critical
questions posed by Hunter et al. (1986) in their watershed review.
V. THE PROBLEM OF ATTACHMENT
The development of new electronic tagging technologies, many of which re-

quire the tag to remain on the fish for periods of months to many years, has pre-
sented researchers with the challenge of developing new methods of attaching tags
in such a way that they do not affect the behavior, do not adversely affect survi-
vorship, and do not fall off.
Over the years, acoustic tags have been attached successfully to tunas in many
different ways-for example, harpooned into free-swimming fish (Carey and
Lawson, 1973); strapped to the dorsal musculature (Holland et al., 1990); with
anchors implanted into the dorsal musculature (Block et al., 1997; Brill et ul.,
1999; Dagorn et al., 2000); inside the stomach, either free or attached to special
“hooks” to provide longer retention (Yuen, 1970; Davis et al., in press); or intra-
peritoneally (Klimley and Holloway, 1999). However, because tracking studies
generally last for only a few hours to days, the long-term retention of the tags and
their effects on survivorship have rarely been examined. Klimley and Holloway
(1999) found acoustic tags placed into the peritoneal cavity of yellowfin tuna re-
mained in place for 9 months, and presumably did not affect the survivorship.
Early experiments with archival tags compared the long-term retention of ex-
ternal and intraperitoneal placements (J. Gmm and T. Davis, CSIRO, unpublished
data). In these experiments, 100 of each of the two types of tags were deployed
on juvenile SBT in southern Australia. The return rate for the intraperitoneal
tags was 8% (approximately the same return rate as conventional tagging studies
conducted at the same time), with tags returned after periods of liberty of 3-
24 months. No external tags were reported recaptured, and the conclusion drawn
was that the external placement had caused mortality in the tagged fish.
Gunn et al. (1994) adopted the intraperitoneal placement throughout their
SBT archival tagging program, which has had recapture rates of > 15% from 5 14
releases. The recapture rates for archival tags are higher than those for conven-
tional tagging releases conducted at the same time on fish of the same cohorts
(CSIRO, unpublished data), suggesting that reporting may be higher, and/or shed-
ding of internal tags may be lower. Similarly Block and colleagues have also used
intraperitoneal placement for archival tagging Atlantic bluefin and have approxi-
mately a 16% recovery rate from 279 releases. Intraperitoneal placement has the
advantages that tag shedding appears to be zero and, where the species has a vis-
ceral rete, it is possible to determine when a fish has eaten from the internal tem-
perature sensor archival tag data (Gunn et al., 2001).
Brill et al. (1997) also conducted experiments with intramuscular placement
of archival tags. These were conducted with scaled-down dummy tags in an
aquarium and proved long-term retention is possible, along with quick healing of
the wound if the tag is directly inserted into the dorsal musculature, rather than
making a deep incision.
Tags that are to be carried for a long period require insertion and acceptance
of a foreign object into the fish (the applicator dart), and placement that avoids
direct injury to the animal. The preferred placement for PAT tags on tunas is at
the base of the second dorsal fin. Experiments on captive fish with early genera-
tions of the dummy PAT tags demonstrated that tags placed close to where the
body narrows posterior to the second dorsal fin, had minimal contact with the
body and did not disturb normal swimming patterns. Also, at the base of the sec-
ond dorsal fin there are a series of bony processes which provided an ideal site to
secure the anchor. The pop-up tags were initially designed to be placed in this
position to avoid interaction with the body of the animal. Short stiff leaders con-
structed with extra-hard 1.8-mm-diameter monofilament have provided optimal
results on Atlantic and Pacific bluefin tuna, blue marlin, and lamnid sharks. The
leaders are crimped with stainless steel sleeves and are coated with shrink wrap to
protect the fish from injury from the monofilament and sleeves as well as to in-
crease the stiffness of the leader. The general concept is to have the tag lifted off
the surface of the fish by the short, stiff leader with the additional aid of the buoy-
ant float. In the case of the Wildlife Computers-constructed PAT tags, floats used
for Atlantic bluefin tuna are larger than the original floats designed for the single-
point tags (Block et al., 1998b). Large bluefin are capable of carrying the extra
drag and the increased buoyancy pulls the instrument package off the body of the
fish. This prevents as much as possible tag and fish interaction, which is most
likely the leading cause of PAT tag failure to transmit. From controlled studies in
the laboratory, the most severe interaction occurs at the point of attachment and at
the maximum width of the float. Together these two areas can cause large subder-
ma1 injuries that can cause mortality.
In all attachments, the critical factor is to achieve a deep insertion (IO-12 cm
in a large fish; 7.5 cm in a small fish) of the applicator dart across the pterygio-
phores. Once inserted correctly, few darts of any type will pull out. Over-the-side
applications are more difficult due to the challenge of exact placement of the tag
into the desired position. Two types of anchor materials are often used: titanium
darts and medical grade plastic darts. In studies on the Atlantic and Pacific bluefin
tuna, conducted on both captive and wild caught bluefin, the flat-head titanium
dart retained with high reliability (no premature release from over 60 deploy-
ments). Nylon darts in our experiments showed poor retention both in the lab
and in the field for long durations; however, some studies have had relatively
high success with these darts although it would be difficult to know if tags were
on for long durations without a continuous temperature archive (Lutcavage et ~1..
1999a).
VI. THE FUTURE OF ACOUSTIC, ARCHIVAL,

AND POP-UP TAGGING
A. Technology
The exciting results recently achieved with the latest generations of pop-up
archival satellite tags begs the question as to whether this will become the tagging
technology of choice for tunas in the 21 st century, making the other technologies
redundant. Our feeling is that pop-up satellite archival tags are going to revolu-
tionize what we know about tunas. However, all three electronic tagging tech-
niques have applications that are useful and it is really up to the experimental
questions and the species as to whether or not we can use a particular technology.
Acoustic technology remains the most appropriate tool for studying fine-scale
movements and behavior. When combined with the array of oceanographic mea-
surements possible on modern research vessels, acoustic data provide the user
with an unparalleled opportunity to examine the links between fine-scale oceano-
graphic features and the vertical and horizontal movement of a single fish. Addi-
tionally, for physiological data with high data acquisition rates, the memory of the
archival and PAT tags are not capable of storing the large data sets, so acoustic
technologies remain the only solution (e.g., tailbeat and EMG). Although the cost
of following individual fish has limited the number of acoustic data sets we have
for tuna, their importance cannot be underestimated. We do not need to make large
numbers of these fine-scale observations for them to be useful in interpreting what
tuna are doing in their open ocean environment. As they have for bigeye and
southern bluefin, acoustic data provide a valuable basis for interpretation of longer
term, but less detailed, data sets collected by archival or pop-up archival satellite
tags. Three foci on which more acoustic observations would be very useful are:
l Tuna in open ocean habitats, where directional movement and behavior are
unlikely to be influenced by topographic features or FADS
l Tuna within schools to provide a better understanding of the dynamics of
individuals within schools
l Feeding activity to identify how this differs from searching or traveling
behavior
As the most recent version of the pop-up satellite archival tags can be down-
loaded if the fish is recaptured prior to pop-off, and thereby provide data similar
to those collected by archival tags, the choice of whether to use archival or pop-
up tags will depend heavily on the fish you are planning to tag and the objectives
of the study:
l What is the probability of recapturing the jish.7 If the probability is low,
regardless of other issues, pop-up tags provide the best option for obtaining
data. Archival tags currently sell for around U.S. $1400-$1800, and pop-up
tags for U.S. $3X-$4500. If one expects a 10% return rate for archival
tags, each tag data set costs on the order of $14,000-$18,000. If one as-
sumes a 100% success in pop-ups, the cost per data set is $3500 -$4500.
l What temporal scale is the hypothesis testing? Currently, only archival tags
are capable of collecting data for periods of much more than 1 year. Until
upload rates to ARGOS (or similar new generation) receivers are improved,
the trade-off between data logging life and the amount of data that can be
transmitted suggests that for long-term experiments archival tags would be
the best option. The long-term attachment of a pop-up tag is unproven and,
particularly in tropical areas, marine fouling may make this difficult.
Additionally, if one wishes to collect data on feeding behavior, an internal
temperature sensor is required and an archival tag is the preferred choice.
l What resolution is required in the spatial data.? In terms of their ability to
deliver accurate information using light-based geolocation, archival tags
5. ADVANCES IN TAGGING OF Tl’hAS 217
currently outperform pop-up satellite archival tags. While both use light to
estimate geolocation, the archival tag, with the ability to examine all the data
stored in memory, allows the user more flexibility and power in estimating
longitude and latitude. The current pop-up tags each have limitations pri-
marily based on the challenges of delivering data sets back through ARGOS
satellites. If a tag comes up in bad weather or hits a beach shortly after sur-
facing, little to no data will be returned. The PAT tag is capable of delivering
geolocation for the duration of the mission: however. memory limitations as
well as current software will limit this to at most a 1.2-year record.
l What size tuna are you tagging? Archival tags have been deployed on tunas
as small as SO-cm FL (Japanese National Research Institute of Far SeasFish-
eries, unpublished data), and although pop-up tags have been successfully
used in a short deployment on an l&kg albacore (B. Block, unpublished
data), the current designs arc best suited for much larger fish, particularly
if long-term deployments are required. Lotek Wireless, Inc., of Canada is
currently testing an archival tag small enough to deploy on 30-cm FL
tunas, which will allow researchers to study behavior and movement of
young-of-the-year tuna. If the objective of the study is to study juvenile
fish, or to examine ontogenetic changes in behavior and movement, archi-
val tags currently provide the best option. As manufacturers reduce the siLe
of pop-up satellite tags substantially over the next few years, they will no
doubt increase the utility of this form of electronic tagging on smaller
individuals.
There are a number of important improvements that would make archival and
pop-up tags more useful.
First, they need to be made more robust. The failure rates experienced by users
of both technologies over the last few years are perhaps to be expected given the
rapid speed of development and the many unknowns regarding tuna behavior
(how deep they dive, what temperature extremes are they likely to experience,
etc.). However, as the technology matures, it is essential that these failures are not
repeated. It is in the interest of the manufacturer and researcher alike for this to
happen as funding agencies tend to balk at researchers who repeatedly have to
make apologies for failed equipment.
Second, manufacturers have to be willing to collaborate in studies validating
the hardware and software they produce. As geolocation is a critical feature of
both technologies. it is essential that researchers have access to data and software
that allows them to independently validate the estimates of position being pro-
duced by tags. To accept positions produced by tags or by software used to am-
lyr,e the data without adequate validation of the methods is poor science.
Third, while current Wildlife Computers tags provide evidence of premature
release of the tag or fish mortality, all pop-up tags of the future must provide
researchers with an ability to tell whether a fish has died while carrying the tag, or
if the tag has become detached and floated to the surface. The former would be
invaluable in examining postrelease mortality, and even natural mortality over
long time scales if pop-up tag life can be extended.
B. The Future Application of Electronic Tags and

Integration of Data into Spatial Dynamics Models
Over the last decade the application of acoustic, archival, and pop-up satellite
tag technology has contributed significantly to our understanding of the move-
ment, behavior, biology, and physiology of a number of tunas species. For south-
ern bluefin and Atlantic bluefin in particular, electronic tags have provided some
quantum leaps in our understanding of the timing, directionality, and seasonality
of movement; the residence times in different parts of their range; and the links
between these and environmental factors. We have been able to determine how
often these fish eat, and perhaps in the future we will also be able to determine the
amount of food eaten each day (Gunn et al., 2001). These parameters remain
largely unknown for yellowfin, bigeye, albacore, and Pacific bluefin, and as such
represent critical uncertainties in the assessments of these species (Hunter et al.,
1986). We still require resolution of the stock structure of bluefin in the Atlantic,
and bigeye and yellowfin in the Pacific and Indian oceans. To correctly standardize
the catch per unit of effort indexes of abundance that are the central plank of most
stock assessments, we urgently require a better understanding of the horizontal
and vertical distributions of all tuna species, and how these are affected by oceano-
graphic variation.
Encouragingly, the successful applications of archival tags, pop-up archival
tags, and acoustic listening stations over the last decade have demonstrated that
we now have the tools to reduce uncertainties. Archival and pop-up tagging of
Pacific bluefin and bigeye has begun, and is already showing promising results
(T. Itoh et al., unpublished data; Marcinek et al., 2001). Similarly, pop-up tagging
has begun on southern bluefin, Pacific bluefin, yellowfin, and albacore. There is
every reason to expect that these studies will provide similar advances to those we
have seen for the bluefin species.
Electronic tagging programs, from tracking individual fish to attaching pop-
up tags to hundreds of large adult bluefin tuna, are relatively costly. Yet the ad-
vances made in the last few years suggest that returns on investment in these
studies are substantial. It is important to recognize that electronic tags alone will
not provide all of the answers to our questions on tuna movement and habitat
preferences. There is also a demonstrable need to conduct well-designed, large-
scale conventional tagging programs that will provide the large sample sizes of
coarse-scale data on movement along with estimates of exploitation rates, mixing
rates, and growth. Combining genetic data with electronic tagging data provides
increasing opportunities to compare contemporary movements with historical pat-

terns of phylogeography.
In the near future, it seems likely that the integration of movement and behav-
ioral data from conventional and electronic tagging studies with remotely sensed
and observational oceanographic data on ocean temperature, color, and height will
provide the basis for meaningful models of the movement dynamics of popula-
tions or stocks. To date no one has attempted this multidisciplinary integration.
However, Sibert and Fournier (2001) have examined the potential for using the
concepts of a biased random walk and diffusion-advection equations as a basis
for integration of conventional and electronic tagging data, with promising re-
sults. Advection-diffusion models have also been successfully used with oceano-
graphic data in the analysis and interpretation of the large-scale movement and
distribution of tunas (Lehodey et ul., 1997, 1998; Maury and Gascuel, 1999).
The imperative for addressing the uncertainties in tuna movement dynamics,
stock structure, and the influence of the environment on recruitment and produc-
tion has never been greater, particularly in heavily or overexploited stocks. Given
due attention, allocation of adequate resources for well-defined research projects.
and a multidisciplinary approach, the advances in tagging technology and mod-
eling techniques over the last decade mean we are better placed than ever to ad-
dress these critical issues.
ACKNOWLEDGMENTS
The preparation of the manuscript benefited from the contributions of the Tag-A-Giant scientific
team. We thank, Andreas Walli. Susanna Blackwell, Heidi Dewar. Tom Williams, Andre Boustany,
Eric Prince, and Charles Farwell. Many others made the research possible. The Atlantic bluefin tuna
research described herein was primarily supported by the NMFS, NSF. the Packard, Pew, MacArthur
and Monterey Bay Aquarium Foundations. The southern bluefin tuna research has involved contribu-
tions from a large team of CSIRO researchers. notably Jason Hartog, Simon Wotherspoon, Andrew
Betlehem, Tim Davis, Naomi Clear, and Tom Polacheck. The archival tag research was supported by
the Australian Fisheries Management Authority and the Japan Marine Fishery Resource Research
Centre. and industry associations in Australia and Japan.
REFERENCES
Anonymous (1996). IUCN red list of threatened animals.

Anonymous (1998). Report of the fourth meeting of the scientihc committee, Tokyo, Japan.
Block. B. A., Keen. J. E., Castillo, B., Dewar, H., Freund, E. V., Marcinek, D. J., Brill, R. W., and
Farwell. C. (I 997). Environmental preferences of yellowfin tuna (7’hunnus albacnres) at the
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6
REPRODUCTIVE BIOLOGY OF TUNAS

KURT M. SCHAEFER
1. introduction
II. Gonadal Development
A. Ovaries and Oogenesis
B. Testes and Spermatogenesis
III. Maturation
IV. Spatiotemporal Spawning Patterns
V. Spawning Behavior
VI. Spawning Frequency
VII. Fecundity
VIII. Sex Ratios
IX. Reproductive Energetics
X. Concluding Remarks
I. INTRODUCTION
Comprehensive reviews on the anatomy and physiology of reproduction in

teleosts can be found in previous volumes of this series, including the classic by
Hoar (1969), and the two-part volume on fish reproduction (Hoar et al., 1983).
This chapter is intended to provide an overview and perspective of our present
understanding of some aspects of the reproductive biology of tunas which are
fundamental to fisheries science. The taxonomic nomenclature used throughout
this chapter follows that of Collette et ~1. (this volume). AllothunnuLsfullai, al-
though considered the most primitive member of the tribe Thunnini, will be ex-
cluded from this chapter and from references to the reproductive characteristics of
the tunas.
Tunas are predominantly dioecious, and there appears to be no sexual dimor-
phism in external morphological characters. Tunas are oviparous, have asynchro-
nous oocyte development, and are considered to be multiple or batch spawners,
shedding their gametes directly into the sea, where egg fertilization occurs (Wal-
lace and Selman, 1981; de Vlaming, 1983). Spawning patterns within the tribe
226 KURT M. SCHAEFER
are diverse and complex. There are three types of spawning patterns exhibited by
the tunas: (1) confluent throughout tropical and subtropical regions (Kutsuwonus
pelamis, Thunnus albacares, and Thunnus obesus), (2) regionally confined and
protracted (Auxis spp., Euthynnus spp., Thunnus atlanticus, and Thunnus tong-
gal), and (3) migratory and spatiotemporally confined (Thunnus alalunga, Thun-
nus maccoyii, Thunnus orientalis, and Thunnus thynnus). Common to all these
species within the tribe is the relationship between spawning activity and sea-
surface temperatures in excess of about 24°C. Because of their mode of reproduc-
tion, repetitive broadcast spawners, tunas must have very high lifetime fecundities
to be successful. This is achieved through various degrees of protracted spawning,
along with a combination of high spawning frequencies and relative batch fecun-
dities. For nearly all species investigated, males attain greater sizes than females,
which is the opposite of what is observed for most marine fish.
The reproductive characteristics of a stock along with those of growth and
mortality are among the most important factors in determining the regenerative
ability of a population (Quinn and Deriso, 1999). Understanding the reproductive
biology of tunas and quantifying size-specific parameters provides the means,
when incorporated into length- and/or age-structured models, for predicting the
effects of fishing on the reproductive potential of a stock. Although there has been
some progress in the past 20 years on elucidating some important life history
processes in tunas, for the majority of the species our knowledge regarding repro-
ductive patterns and parameters is meager. Accurate interpretation and classifica-
tion, in recent years, of reproductive condition and estimates of spawning poten-
tial for tunas have largely been the result of utilizing histological techniques and
appropriate classification criteria (Grier, 198 1; Wallace and Selman, 1981; Hunter
et al., 1985; Hunter and Macewicz, 1985a; Schaefer, 1998). Most of the investi-
gations conducted on reproductive biology of tunas in the past 50 years have,
unfortunately, utilized inaccurate methodologies for assessing reproductive pa-
rameters and the spawning potential of stocks.
II. GONADAL DEVELOPMENT
Tunas, like all other scombrids, are primarily heterosexual. However, a few
instances of hermaphroditism have been reported for Katsuwonus pelamis, in
which both testicular and ovarian tissues were observed in the gonads of the same
fish (Raju, 1960; Uchida, 1961).
The paired, elongate, gonads are suspended by mesenteries inside the ab-
dominal cavity, and extend almost the entire length along the dorsal wall of the
coelom. The gonads develop from relatively small, inconspicuous structures into
large masses. The gonads are fused caudally where the cavities join to form a short
duct that terminates at the external opening in the anal region (Bara, 1960; Hoar,
6. REPRODUCTIVE BIOLOGY 227
1969; Harder, 1975). The paired gonads are nearly symmetrical, although there
are some differences in sizes, wi# the right ovary and testis being larger than the
left within some species (e.g., Thrwwursalahga; Ratty et aZ., 1990).
Most studies of gonadal development in tunas, intended to describe maturation
and spawning distributions, have been based on ovaries and have utilized various
formulations of the gonosomatic index for classification of condition (Yuen,
1955; Schaefer and Orange, 1956; Urange, 1961; Kikawa, 1962,1966). If a gon-
osomatic index is calibrated, for instance, through use of histology, it can poten-
tially be used for determination of spatiotemporal spawning distributions, but it is
not accurate for classification of maturity or reproductive activity (de Vlaming
et al., 1982). Other methodologies which are appropriate for interpretation and
classification of the gonadal development and reproductive activity of individual
fish (West, 1990) include the use of oocyte diameters from the most advanced
batch of oocytes present in an ovary (Btiag, 1956; Yoshida, 1966; Schaefer,
1987; Ramon and Bailey, 1996) and histology of ovarian and testicular tissues
(Cayrk and Farrugio, 1986; Goldberg and Au, 1986; Hunter et al., 1986; McPher-
son, 199 1; Nikaido et al., 1991; Batatyants, 1992; Timohina and Romanov, 1996;
Farley and Davis, 1998; Schaefer, 1998). Histological examinations of micro-
scopic slides of ovarian and testicular tissues provide the greatest precision for
classification of reproductive state of tunas (Schaefer, 1998).
A. Ovaries and Oogenesis
Undeveloped tuna ovaries are round in cross-section, and if excised will roll
smoothly between the fingers due to the presence of a lumen. Developed ovaries
are fusiform (spindle-shaped), yellowish in color because of the presence of yolk,
and circular in cross-section.
Tuna ovaries are considered asynchronous because oocytes in various devel-
opmental stages are present in the ovary simultaneously (WaIlace and Selman,
1981; de Vlaming, 1983). This is definitive of fish which spawn numerous times
during a single protracted spawning season. The histological classification of tuna
ovaries for assessments of reproductive biology should be based on the system of
Hunter and Macewicz (1985a), as modified by Schaefer (1996, 1998). Detailed
reviews on this topic for teleosts in general, which are relevant to tunas, are given
by Harder (1975), Wallace and Selman (198 I), Nagahama (1983), de Vlaming
(1983), and Tyler and Sumpter (I 996). A brief description of oogenesis and his-
tology of tuna ovaries is provided here.
Oogenesis begins with the proliferation of oogonia by mitotic divisions within
the oogonial nest, which become primary oocytes (Figure 1A). The oocytes con-
sidered within this developmental category are unyolked. The initial primary
oocyte has a relatively narrow, densely staining basophilic cytoplasm and a large
clear nucleus. The cytoplasm increases in size with oocyte growth, and shows
KURT M. SCHAEFER
Fig. 1. Developmental stages and oogenic cells observed in Thunnus albacares ovaries.
(A) Unyolked oocyte (X 160). (B) Early yolked oocyte (X 100). (C) Advanced yolked oocyte (X40).
(D) Migratory-nucleus-stage oocyte (X40). (E) Hydrated oocyte (X25). (F) Postovulatory follicle
less than 12 h after ovulation (X 160).
differentiation in staining, with inherent lighter oval areas, possible precursors of

yolk vesicles. In the nucleus, multiple nucleoli are distributed around the periph-
ery. This is considered the early perinucleus stage, characterized by the enlarge-
ment of the oocyte, along with an increased number of peripheral nucleoli and the
appearance of lampbrush chromosomes in the nucleus. At this point the oocyte is
surrounded by an inner layer of granulosa cells and a thin flat layer of thecal cells.
The oocytes next enter a prolonged secondary growth phase in which the enlarge-
ment of the oocyte is caused by formation and accumulation of yolk (vitello-
genesis), which depends on pituitary gonadotropin (Ng and Idler, 1983). The yolk
vesicles are the first strnctures to appear in the oocyte cytoplasm, distributed at
first in a peripheral position in the ooplasm and then subsequently spreading to-
ward the perinuclear zone. Yolk granules begin to appear and replace the majority
of the yolk vesicles (Figures 1B and 1C). There are three distinct types of struc-
tures within the cytoplasm during vitellogenesis: yolk vesicles, yolk granules, and
lipoid vesicles.
In early yolked oocytes (Figure 1B) numerous euvitelline nucleoli appear ho-
mogeneously around the nuclear membrane, with no true nucleolus present. There
is an increase in the lipoid vesicles and yolk granules, and the zona radiata can be
distinguished in the follicular epitbelium as development proceeds (Figure IC).
In the more advanced stages of vitellogenesis, where the oocytes are advanced
yolked, sharply staining yolk granules occur throughout the ooplasm, along with
larger lipoid vesicles.
Vitellogenesis ceases once these oocytes are fully developed, and eventually
undergo maturation and ovulation after an appropriate hormonal stimulation
(Masui and Clarke, 1979; Wallace and Selman, 1981). The first observed histo-
logical change associated with the final maturation of the oocyte is the migration
of the nucleus (germinal vesicle) toward the animal pole where the micropyle is
located. During this process coalescence of the lipoid vesicles takes place within
the cytoplasm (Figure 1D). After the germinal vesicle reaches the animal pole, the
membrane of the germinal vesicle disintegrates and its contents become confluent
within the cytoplasm. Early hydration of the oocyte begins at this time with the
initiation of the fusion of the yolk granules to form yolk plates. The final matura-
tion of the oocyte occurs during the later stage of hydration when the yolk plates
completely fuse and form a homogeneous yolk mass (Figure lE), during which
time the oocyte significantly increases in size due to hydration or the uptake of
fluid by the oocyte (Wallace and Selman, 1981). This fusion of yolk granules and
hydration gives the oocyte a translucent (hyaline) appearance in fresh or preserved
whole oocytes (Schaefer, 1998).
Upon completion of maturation the hydrated oocytes are expelled through a
rupture in their surrounding follicles into the ovarian lumen. The postovulatory
follicle remains as a distinct involuted structure within the ovigerous lamellae. and
consists of an inner epithelioid layer of granulosa cells and an outer connective
tissue layer of thecal cells. The postovulatory follicle is transitory (Bara, 1960;
Yamamoto and Yoshioka, 1964; Hunter and Goldberg, 1980; Goldberg rt NI.,
1984), and in Katsuwonus pelamk and Thunnus albacares, by 24 h after ovula-
tion, postovulatory follicles cannot be accurately identified (Hunter et a/., 19x6;
Schaefer, 1996). At the time of spawning the new postovulatory follicles have an
involuted shape, with numerous folds and a relatively open follicular cavity. The
granulosa epithelioid cell layer lining the lumen shows regularly aligned cuboidal
to columnar cells with prominent basal nuclei. The tbeca is now about the same
thickness, and in only loose contact with the granulosa. The degenerating posto-
vulatory follicle is smaller, has fewer involutions, and has a follicular cavity (Fig-
ure 1F). A thick thecal layer now surrounds the relatively thin granulosa cell layer,
and the two layers are in much closer contact. Degenerating cells of the thecal and
granulosa layers have sharply staining pycnotic nuclei, and an irregular alignment
of the cell walls and nuclei (I-lunter et al., 1986; Schaefer, 1987, 1996, 1998).
B. Testes and Spermatogenesis
Undeveloped tuna testes are relatively flat in cross-section, and if excised do

not roll smoothly between the fingers because they are solid, apart from a longi-
tudinal sperm duct (vas deferens) medially, which can be seen with the unaided
eye if the testis is illuminated. Developed testes are somewhat flattened and white
in color because of the presence of milt. Tuna testes are considered as an unre-
stricted spermatogonial testis type, because the distribution of spermatogonia may
occur along the entire length of the tubule (Grier, 1981). The histological classi-
fication of tuna testes development should be based on the degree of spermato-
genesis as described by Crier (1981) and the classification system of Schaefer
(1996, 1998) for assessments of reproductive biology. Detailed reviews on this
topic (for teleosts in general) which are relevant to tunas are given by Grier (198 1,
1993) and Nagahama (1983). A brief description of spermatogenesis and his-
tology of tuna testes is provided here.
Each lobe of tuna testes is composed of interstitial and germinal (lobular)
compartments. The germinal compartments are situated within lobules that radiate
perpendicularly from the vas deferens or efferent duct and terminate at the periph-
ery of the lobe, the tunica albuginea. The lobules are separated by interstitium
composed of fibrous connective tissue. The lobular compartments containing the
germ cells are lined peripherally by specialized somatic cells referred to as lobule
boundary cells (Nagahama, 1983). These lobule boundary cells are considered to
be homologous with Sertoli cells, and often occur in close proximity to spermatids
and developing sperm, and appear to be involved in phagocytosis of degenerating
germ cells and transport of metabolites (Grier, 1981; Nagahama, 1983).
During maturation, all germ cells within a cyst are at about the same stage of
development. The four cellular stages that can be differentiated in sperm matura-
tion are spermatogonia, spermatocytes, spermatids, and spermatozoa (Figures 2A,
2B, 2C, and 2D). Primary spermatogonia, distributed along the lobule lengths,
undergo a series of mitoses which produce cysts containing several spermato-
gonial cells, called secondary spermatogonia. The primary spermatogonia are
spherical and acidophilic, possess a single prominent nucleolus in each, and are
the largest germ cells in the testis (Figure 2A). A second series of mitotic divisions
6. REPRODUCTIVE BIOLOGY
Fig. 2. Developmental stages and spermatogenic cells observed in Thunnus ulhaccrres testes.
(A) Primary spermatogonia (SC? x240). (B) Primary spermatocyte (PS) cells and secondary sper-
matocytc (SS) cells (X240). (C) Spermatids (SM; X240). (D) Spermatozoa (S: X240). (E) Prespawn-
ing stage in mature testis with vas deferens tilled with spermatozoa (X 10). (F) Postspawning stage
(< 12 h) in mature testis with the vas deferem almost completely devoid of spermatozoa (X 10).
results in the formation of cysts full of primary spermatocytes. These stain baso-
philically, have more condensed nuclei. and are smaller (Figure 2B). The next
developmental stage in the maturation process is secondary spermatocytes (Fig-
ure 2B) which are formed after the first meiotic division, and are retained within
the cysts until they eventually burst through the cyst’s capsule into the lobular
lumen, where they develop after a second meiosis into spermatids. Each spermatid
develops into a spermatozoon, a process termed spermiogenesis. A spermatid has
a condensed and intensely staining basophihc nucleus (Figure 2C). Mature sper-
matozoa possess a distinct rounded basophilic head and a long acidopbilic flagel-
lum (Figure 2D). An electron micrograph of an individual sperm from Z’hunnus
akzlunga is shown in Ratty et al. (1990).
The lobular lumens are continuous with the vas deferens, which are straight
tubes with thick, muscular walls, which merge caudally and exit through a pore
in the anal region. The lumen of the vas deferens is lined along its length with
cuboidal to columnar epithelium, and varies in general appearance from smooth
to convoluted (Harder, 1975; Schaefer, 1996). Histological evidence of recent
spawning activity in male Thunnus albacares is apparently detectable for only
about 12 hours after the spawning event, based on appearance of the epithelial
lining and the amount of sperm present in the vas deferens (Figures 2E and 2F;
Schaefer, 19%).
III. MATURATION
An individual tuna must reach a minimum size or age before it is physiologi-

cally capable of initiating full gametogenesis in response to the appropriate envi-
ronmental cues. The size and/or age at which a certain fraction (e.g., 50%) of a
population of tunas reaches maturity, and is thus capable of reproducing, is an
important life history parameter. Unfortunately, this concept has not received suf-
ficient attention nor proper evaluation. There has been a considerable amount of
nonquantitative estimation of sizes and/or ages at maturity for tunas based mostly
on invalid gonosomatic indexes (de Vlaming et al., 1982). Many such studies have
reported the apparent size at first maturity. That value is equivalent to the mini-
mum size individual, sampled from a population, observed to be sexually mature.
Reporting only the size at first maturity is useless, and even misleading. It is the
functional statistical relationships between proportion mature and size and/or age
which need to be derived to estimate proportions mature from a population.
The first requirement in the process of the estimation of proportions mature is
to define precise criteria for the classitication of maturity. Histological examina-
tions and criteria are necessary to attempt to correctly classify female and male
tuna as to sexual maturity. Particularly for females, histological information is
required because of the inadequacy of gonad indexes or oocyte diameters for sepa-
rating developing ovaries, in a stage of early vitellogenesis, from postspawning
ovaries, in atretic stages of resorption. The histological classification scheme used
by Schaefer ( 1998) for female and male Thunnus albacares provides the basis to
distinguish between mature and immature individuals, Females classified as ma-
ture can be classified as reproductively active or inactive. Females are classified as
active when the ovary contains advanced yolked oocytes, and there is no atresia
or only minor alpha atresia present. Females classified as mature-inactive have
ovaries with oocytes in developmental stages of either unyolked or early yolked,
and also contain alpha atresia of yolked oocytes and/or beta atresia. Also included
in this class are ovaries with advanced yolked oocytes, of which more than 50%
are atretic. The immature class consists of females whose ovaries contain un-
yolked or early yolked oocytes, but no signs of atresia. Males are classified as
mature if there is histological evidence of sperm in the sperm duct and immature
if there is no sperm in the sperm duct.
The second consideration is the implementation of an appropriate experimen-
tal design based on previous knowledge of the spawning locations and times for
the species under consideration. Probably the most limiting factor in most studies
of the reproductive biology of tunas, particularly estimation of maturity, is the
difficulty in obtaining suitable tissues from specimens over a desired size range to
encompass immature to 100% maturity during the period of reproductive activity.
This can be further complicated by potential gear avoidance and biases caused by
gear selectivity as a result of vertical stratification of individuals in different repro-
ductive states (Suzuki, 1994; Davis et al., 1998).
The final consideration should be the use of an appropriate statistical proce-
dure for evaluation and interpretation of the data included in the experimental
design. A weighted nonlinear predictive regression model fit directly to these sig-
moidal data is probably the most appropriate (Schaefer, 1987, 1998). The model
can then be used to predict proportions mature at specific lengths and/or ages for
the stock being investigated.
The available estimates of lengths at 50% maturity of female tunas are given
in Table I. These estimates, for just 3 of the 15 species of tunas, appear to be the
only reliable estimates available at this time. For some of the other species there
are estimates of the lengths, and in some instances presumed ages. at first maturity.
Table I
Estimates of Lengths at SO% Maturity for Female Tunas
L,ength
Specie\ (cm1 AK2 Reference
47 Eastern Pacific Schaefer (1987)

42 Atlantic Cayrk and Farrugio f 1986)
-17 Western Indian StCquert and Ramcharrun (1996)
13 Western Indian Timohina and Romanov ( 1996)
I ox Western Pacific McPherson ( I991 )

Y,2 Eastern Pacitic Schaefer ( 1998)
However, most all of those estimates are based on invalid methodologies and clas-
sification criteria.
For Auks spp. and Euthynnus spp., which have been investigated in various
oceans of the world, there is a limited amount of information regarding matura-
tion. Yesaki and Arce (1994), summarizing investigations based on gonad indexes
and anatomical scales, report the length at 50% maturity for Auxis thazard from
the Gulf of Thailand to be 34 cm, and lengths at 50% maturity for A. thazard and
Auxis rochei off India to be 30.5 and 24 cm, respectively. Yesaki (1994a) reports
the apparent length at 50% maturity for Euthynnus afinis off India, based on an
investigation using an anatomical scale, to be 43 cm. Although there are reported
lengths at first maturity for Euthynnus alletteratus based on gonosomatic indexes
(Yoshida, 1979) there do not appear to be any estimates of lengths at 50% matu-
rity. The relationship between proportion of female Euthynnus Zineatus mature
and length from the eastern Pacific (Schaefer, 1987) is given in Figure 3, and the
estimated length at 50% maturity in Table I.
The estimated lengths at 50% maturity given in Table I for female T albacares
from studies conducted in two different oceanic regions are quite variable. These
differences may be more a function of the experimental designs and classification
procedures employed than geographic variation. The relationship between pro-
portion of female 7: albacares mature and length from the eastern Pacific is given
in Figure 3. In the study by Schaefer (1998) the estimated length at 50% maturity
20 40 60 60 100 120 140 160

LENGTH IN CENTIMETERS
Fig. 3. Relationships between proportion of female tunas mature and length: (I) Katsuwonus
pekmis (StCquerr and Ram&u-run, 1996), (2) Euthynnus lineafw (Schaefer. 1987), and (3) Thurmus
alhacares (Schaefer, 1998).
for females of 92 cm corresponds to an age of about 2 years (Wild, 1986). As an

example of the size at first maturity, and the potential misuse of such information,
the minimum length at sexual maturity of females was 59 cm. Males were found
to mature at lesser lengths than females, with an estimated length at 50% maturity
for males of 69 cm. For both sexes, there were statistically significant differences
in annual and geographical estimates of lengths at 50% maturity. In the eastern
Pacific 7: alhacares and Katsuwonus pelamis were found to mature at lesser sizes
off Central America than in the northern areas off southern Baja California. the
southern part of the Gulf of California, and the Revillagigedo Islands (Schaefer
and Orange, 1956; Orange, 196 1).
The relationship between proportion of mature female K. pelamis and length,
from the Indian Ocean, is given in Figure 3. The shape of the maturation curve is
noticeably different than that for 7: albacares, but similar to that for E. lineatus. It
appears that in K. pelamis and E. lineatus, once the critical size and/or age is
attained, there is a strong selection pressure for individuals to initiate maturation.
The estimated lengths at 50% maturity given in Table I for female K. pelamis from
studies conducted in two different oceanic regions are almost identical. In the
study by Timohina and Romanov (1996), the estimated 43-cm length at 50% ma-
turity for females reportedly corresponds to an age of about 1.5 years. In this same
study males were reported to mature at lesser lengths than females, with the esti-
mated length at 50% maturity for males being 40 cm. However, in the other two
studies (Cayre and Farrugio, 1986; Stequert and Ramcharrun, 1996) males were
reported to be slightly larger than females at 50% maturity. These differences are
probably a result of the criteria used for classification of maturity. I expect that
male K. pelamis, as observed for male 7: alharrzres (Schaefer, 199X), become
functionally mature with sperm present in the sperm duct before the females are
capable of reproducing.
There is a very limited amount of information available on size and/or age at
maturity in Thunnus thyznus. A maturity schedule based on valid histological
criteria has not been derived. A study was conducted by Baglin (1982) in the
western Atlantic to derive information on reproductive biology, including size and
age at maturity, but mature fish were not obtained. Rodriguez-Roda (1967) con-
ducted research on the reproductive biology of eastern Atlantic and Mediterranean
7: th~nnus, but had a very small sample size upon which conclusions were based
regarding size at maturity. Regardless of these inadequate experimental designs
and invalid conclusions for 7: thymus, subsequent researchers have accepted the
age of 100% (knife edge) maturity for the west Atlantic to be IO years of age
(200 cm), and 5 years of age (130 cm) in the eastern Atlantic (Clay. 1991; Mag-
nuson et rtl., 1994).
Even less research has been carried out on reproductive biology of Thunnus
orientalis in the Pacific Ocean. and size and/or age at maturity is poorly under-
stood. However, since 1970 at Kinki University, Oshima Experimental Station,
Japan, studies on the aquaculture of 7: orientalis have been conducted. Five-year-

old fish spawned in a tank for the first time in 1979. A group of about 200 7-year-
old fish spawned in captivity in 1994 at this facility in cages, and have continued
to spawn seasonally. In 1998 at the Japan Sea Farming Association Amami Sta-
tion, ?: orientalis estimated to be 10 years old began spawning (Lee, 1998). Al-
though these observations for captive T. orientalis indicate that spawning has
occurred for fish after 5 years in captivity, it is necessary to sample wild fish from
the spawning grounds to derive reliable maturity schedules for the stock.
For Thunnus maccoyii, Warashina and Hisada (1970) reported size at first ma-
turity to be about 130 cm. Campbell (1994), using their data, estimated that the
mean size at first maturity was in the range of 150 to 160 cm. Davis (1995), using
oocyte diameter and gonad index data for southern bluefin tuna caught south of
the spawning grounds, estimated the mean size at first maturity to be 152 to
162 cm. This parameter has been inadequately defined in the past, and is likely to
be upward of around 164 cm (T. Davis, CSIRO, personal communication). The
estimated age for T maccoyii at this length is about 13 to 14 years (Gunn et al.,
1996).
Two other tuna species, Thunnus ulalungu and Thunnus obesus, both of high
commercial value, have also been investigated for obtaining an understanding of
their reproductive biology in various oceans of the world. However, maturity
schedules are not available for either, and there is only some fragmentary infor-
mation on their sizes at first maturity. Thunnus alulungu are reported to reach
sexual maturity in the size range of 85 to 90 cm (Ueyanagi, 1957; Otsu and Han-
sen, 1962) when they are about 6 to 8 years old (Labelle et al., 1993). Thunnus
obesus have been reported to reach sexual maturity at a size of 100 to 130 cm
when they are about 3 years old (Calkins, 1980). These estimates of size at first
maturity, however, should not be considered valid or useful.
For testing hypotheses regarding geographical or temporal variation in sizes
and/or ages at maturity through evaluations of shifts in maturity schedules, or
statistics at 50% maturity, it is imperative that the techniques employed to derive
the parameters are comparable. These should be based on precise methodologies,
such as histology and statistical estimation procedures, including nonlinear mod-
els fit directly to adequate data sets. It is also important for researchers to precisely
specify the histological criteria used for classification as to maturity so as to per-
mit valid comparisons among oceanic regions.
IV. SPATIOTEMPORAL SPAWNING PATTERNS
Current knowledge of spatial and temporal spawning distributions for tunas is

presented in this section. Although larval surveys targeting tunas in appropriate
locations and times can provide fine-scale information on spawning (Davis et al.,
1990; Leis et ul., 199 1; Boehlert and Mundy, 1994). patchiness of tuna larvae
makes this technique inefficient for large-scale spawning distribution surveys

(Ahlstrom, 1971, 1972; Nishikawa et al., 1985; McGowan and Richards, 1989).
Sampling ovarian tissues from adult tunas from commercial or recreational land-
ings is a more efficient process for mapping of spatiotemporal spawning distri-
butions. Histological assessment of all individual female ovarian tissues is not
required for defining general spawning patterns. Gonosomatic indexes or, better
yet, maximum oocyte diameters can be calibrated with histological information
and then used for classification of spawning activity and defining geographical
and temporal spawning distributions (Schaefer, 1987, 1998; West, 1990). In ad-
dition, the presence of residual hydrated and ovulated oocytes in ovarian lumens
is evidence of recent spawning. There are numerous examples in the literature,
based on inadequate sampling of gonads and larvae, which draw conclusions
about the seasonal characteristics of tuna spawning in tropical waters (Stequert
and Marsac, 1986; Fonteneau and Marcille, 1988; Shomura el al., 1994).
Although there are exceptions, it appears that most species of tunas exhibit
year-round spawning patterns in the tropical regions of their distributions, and
spawning is seasonally restricted only in subtropical regions. Four species of the
genus Thunnus (alalunga, maccoyii, orientalis. and thynnus) are the only truly
migratory species of the tribe Thunnini. These species differ in their reproductive
patterns from the other tunas, exhibiting directed seasonal migrations to relatively
discrete areas. Two other species of the genus Tkunnus (atbzticus and tonggo
have relatively restricted geographical, but not temporal, spawning distributions
as a result of their distributional ranges in the western Atlantic and the western
Pacific, respectively (Collette and Nauen, 1983). A common factor among the
15 species, excluding Allothunnus ,jhlZui, is that spawning takes place at sea-
surface temperatures of about 24°C and higher, The worldwide spatial extent of
the potential spawning habitat for each species, within its geographical distribu-
tion, can be approximated by the area encompassed by the 24°C surface isotherms
(Figure 4). The northward and southward seasonal movements of the 24°C iso-
therms are responsible for the pronounced seasonal spawning of tunas in the sub-
tropical regions.
Auxis has been observed to spawn throughout its range in tropical and sub-
tropical waters (U&da, 1981). In the eastern Pacific Ocean, Auxis spawning oc-
curs from coastal to oceanic waters throughout the year where sea-surface tem-
peratures remain at around 24°C or higher, and spawning occurs seasonally in
more northern and southern latitudes, correlated with temperature (Klawe, 1963:
Klawe er (11.. 1970; Ahlstrom, 197 1, 1972; Lauth and Olson, 1996). Larvae have
been found over a temperature range of 21.6 to 30.5”C (Richards and Simmons,
1971). In other regions of the world it appears that Auxis spawning distributions
are somewhat restricted to coastal regions (Uchida, 198 1; Nishikawa et al.. 1985).
In the Indian Ocean, Auxis spawning was reported to occur for at least the 8
months during which data were collected (Bogorov and Rass, 1961).
The three endemic species of Euthynnu.s (Collette and Nauen, 1983) spawn
Fig. 4. Seasonal composite distributions of in situ sea-surface temperatures equal to or greater
than 24OC. The boundaries of the shaded areas are the positions of the 24°C isotherms from Levitus
and Boyer ( 1994).
6. REPRODUCTIVE BIOLOGY 2.?cJ
extensively, both geographically and temporally, throughout their respective ranges

(Buiiag, 1956; Marchal, 1963; Richards et al., 1969a.b, 1970; Klawe, 1963; Yo-~
shida, 1979; Nishikawa et ul., 1985; Schaefer. 1987; Lauth and Olson, 19%).
Although spawning distributions of all three species have been reported to bc
restricted primarily to peripheral areas and around islands within their respective
ocean basins (Yoshida, 1979: Nishikawa et al., 1985). spawning in the eastern
tropical Pacific has been shown to be widely distributed from coastal to oceanic
waters (Schaefer, 1987).
Katsuwonus pelamis spawning occurs throughout the year in tropical waters
and seasonally in subtropical waters in all major oceans (Matsumoto et ctl., 1984;
Nishikawa et al., 1985). For the Pacific and Atlantic oceans the latitudinal range
in the spawning distribution has been shown to coincide with the area delineated
on the north and south by the 24°C isotherm (Ueyanagi, 1969: Cayrk and Farru-
gio, 1986). However, K. pelamis larvae have been collected at temperatures as low
as 22°C (Matsumoto et al., 1984; Boehlert and Mundy, 1994). In the western part
of the equatorial Indian Ocean, K. pelamis spawning also occurs throughout the
year, with some apparent periods of greater sexual activity (Stkquert and Ram-
charrun, 1996; Timohina and Romanov. 1996). It was previously assumed that
K. pelamis did not reproduce in the eastern Pacific, but migrated to the central
Pacific to spawn (Rothschild, 1965). This hypothesis has recently been tested, and
the results indicate that significant spawning of K. pdamis occurs in areas of the
eastern Pacific where sea-surface temperatures are equal to or greater than 25°C
(Schaefer, 2001).
Thunnus alhacares, like K. plumis, spawns over vast areas of the Atlantic,
Indian, and Pacific oceans and throughout the year in the warm northern equa-
torial waters, but in the more northern and/or southern regions it is restricted to
the summer months when the sea-surface temperatures exceed 24°C (Nishikawa
et al., 1985; StCquert and Marsac. 1986; Fonteneau and Marcille, 1988; Suzuki.
1994; Wild, 1994). Minimum temperatures where 7: albucares larvae have been
captured with nets are around 24°C (Richards and Simmons, 1971; Boehlert and
Mundy, 1994). Thunnus ulbacares spawning is reported as year-round in warm
waters of the central Pacific (Matsumoto, 1958), but only seasonally near Hawaii
(Matsumoto, 1966). In the eastern Pacific, where spawning of 7: ulbacures occurs
continuously between 0” and 20”N, the proportions of reproductively active fe-
males is positively correlated with fluctuations in elevated sea-surface tempera-
tures (Schaefer, 1998). In that study the minimum temperature at which yellowfin
spawning occurred, based on gonadal histology, was 22°C. although 85.3% of the
spawning took place at temperatures between 26 and 30°C. The expansion of
suitable spawning habitat for 7: dbrrcares in the eastern Pacific with the northward
and southward movements of the 24°C surface isotherms into the subtropical re-
gions north of 20”N and south of 0” during the northern and southern hemisphere
summer months, and the apparent movement of yellowfin into these regions and
subsequent spawning, is possibly the mechanism which generates the two ob-
served cohorts about 6 months apart in the yellowfin length-frequency data for
the population (Schaefer, 1998). Furthermore, interannual events such as El Nino-
La Nina apparently increase and decrease favorable spawning habitat in the east-
ern Pacific, and may be the mechanism for the apparent subsequent increases in
recruitment of juvenile 7: albacares to the population following El Nino events
(Bayliff, 1989).
Thunnus obesus spawning is reported to occur year-round and throughout the
equatorial regions of the Atlantic, Indian, and Pacific oceans (Nishikawa et ul.,
1985; Stequert and Marsac, 1986; Fonteneau and Marcille, 1988; Miyabe, 1994;
Pallares et al., 1998; Stobberup et al., 1998). However, spawning distributions
have been inferred primarily from uncalibrated gonad indexes and larval distri-
butions, which are suspect because of uncertainties in the identification of larvae
of the genus Thunnus (Richards et al., 1990). Although spawning apparently oc-
curs widely across the equatorial Pacific Ocean, the greatest reproductive potential
for 7: obesus appears to be in the eastern Pacific, based on apparent maturation,
size frequencies, and catch per unit of effort (Kikawa, 1966). Kume (1967) re-
ported a correlation between the occurrence of sexually inactive 7: obesus and sea-
surface temperatures below 23 to 24°C. Hisada (1979) reporting on the results of
a study carried out in the Pacific, found that for maturation and reproductive ac-
tivity to occur in 7: obesus requires a mixed layer depth of at least 50 m and a
temperature of at least 24” C.
Thunnus alalunga exhibit distinct northern and southern spawning distribu-
tions and peak seasons as the result of two apparent stocks in both the Pacific and
Atlantic oceans (Nishikawa et al., 1985; Fonteneau and Marcille, 1988; Bartoo
and Foreman, 1994; Murray, 1994). Peak spawning apparently occurs during the
respective northern and southern summer months in oceanic subtropical waters of
the Pacific, centered around 15”N and 15”s latitudes, with a separation of these
zonal regions by a band between 10”N and 10”s where there is limited spawning
observed (Ueyanagi, 1969; Nishikawa et al., 1985). However, spawning does oc-
cur year-round in the northern spawning area of the western Pacific (Nishikawa
et al., 1985) and is apparently protracted over several months in the southern
spawning area as well (Otsu and Hansen, 1962; Ramon and Bailey, 1996). Al-
though the vast majority of spawning in the Pacific appears to occur in the western
and central regions, larvae have been collected in the eastern Pacific as well (Ni-
shikawa et al., 1985). In the Indian Ocean, spawning by 7: ululungu occurs widely
south of about 10”s during at least the period of October to March (Nishikawa
et al., 1985; Stequert and Marsac, 1986). The spawning habitat of 7: alulungu is
characterized by a mixed layer depth to about 50 m and a temperature over 24°C
with no strong thermocline above about 250 m (Ueyanagi, 1969).
Thunnus orient&is spawning in the Pacific is confined to a very restricted
time-area strata in the western North Pacific, relative to their Pacific-wide distri-
butional range (Collette and Nauen, 1983). The spawning occurs t’rorn oft’ the
northern Philippines to central Japan, about 18”N to 35”N, and from the 200-m
isobath of the East China Sea to around 150”E, from April to August. This spawn-
ing area is occupied by the Kuroshio Current. Spawning begins in the south oft
the Philippines in April-May and moves northward to off southern Honshu in July.
Peak spawning is reported to occur in May-June (Nishikawa rt ~1.. 1985; Baylift‘.
1994). Spawning of 7: orientalis also occurs in the Japan Sea during August,
which may consist of a separate stock (Okiyama. 1974, 1979).
In the Atlantic Ocean, where I: thynnus is also widely distributed, spawning
occurs in two relatively restricted locations and times, the Gulf of Mexico in
April-June and the Mediterranean Sea in June-August (Clay, I99 1). In the Gulf of
Mexico it appears that the greatest concentration of spawning occurs in the central
region north of 25”N in May. Thunnus thynnus spawning in the western Atlantic
has also been reported from the Straits of Florida and off the Carolinas (Baglin.
1982; Clay, I99 1). The western Mediterranean and Adriatic seas are considered
spawning areas, but, the greatest spawning apparently occurs between southern
Italy and the Belearic Islands off Spain. Spawning may also occur. however. in the
eastern Mediterranean (Clay, 199 I ).
Thunnus maccoyii spawning is restricted to a relatively small area off north-
western Australia in the eastern tropical Indian Ocean (Nishikawa et L/I., 1985;
Caton. 1991). Spawning is reported to occur in all months except July, although
the main spawning season appears to be from September to April, with a peak in
January and February (Caton. 1991: Farley and Davis. 1998). Adult 71 muccoyii
are distributed globally in waters south of 3O”S, and evidence from tag-recapture
data (Shingu, 1978) suggests that 7: mclccoyii make extensive migrations in the
Southern Ocean. Thunnus mnccoyii. 7: orientcrlis, and 7: thynnus are the best
adapted of all tunas to cold water (Carey, 1973), which permits them to exploit
productive temperate waters. However, like the other tunas. spawning is restricted
to surface water temperatures in excess of about 24°C (Yukinawa, 1987).
Thunnus tonggol has a relatively restricted geographical distribution, being
endemic to the Indo-West Pacific (Collette and Nauen. 1983). Spawning of 7:
tnnggol is reported to be confined to coastal waters, based on the occurrence of
their larvae which were collected at surface water temperatures of 28°C (Nishi-
kawa and Ueyanagi, 1991). It appears there are two distinct spawning seasons for
7: tonggo/ off the west coast of Thailand: a major spawning period during the
northeast monsoon from January to April and a minor spawning period during the
southwest monsoon in August-September. Spawning is also apparently seasonal
for 7: tonggol off Papua New Guinea and off New South Wales, occurring during
the austral summer (Yesaki, 1994b).
Thunnus atlanticus is restricted to the western Atlantic (Collette and Nauen,
1983). Thunnus atlanticus spawning is reported to occur off Miami, Florida. from
April to November (Idyll and de Sylva, 196.3). Spawning has also been docu-
mented in the Gulf of Mexico from May to October (Juarez and Montolio, 1975),
in the Caribbean in March, July, and August (Richards et al., 1974), and around
the Bahama Banks in August (Juarez, 1978).
V. SPAWNING BEHAVIOR
Nocturnal spawning appears to be common among scombrids, as well as other

groups of fishes (Ferraro, 1980; Helfman, 1986). Spawning of Thunnus albacares
at night was reported by Harada et al. (1980) on the basis of running-ripe and fully
hydrated oocytes. Based on oocyte developmental stages and new postovulatory
follicles, the assumption was made that 7: albacares spawn after 2200 h in the
Coral Sea (McPherson, 1991) and i? obesus from about 1900 to 2400 h off Java
and southwest of Hawaii (Nikaido et al., 1991). The times of day at which r al-
bacares spawn in the eastern Pacific were estimated by Schaefer (1996, 1998) by
examining the times of day at which the various reproductive states occur. Spawn-
ing of ‘I: albacares around Clipperton Atoll was determined, on the basis of the
presence of migratory-nucleus and hydrated-stage oocytes and new postovulatory
follicles in ovaries of females sampled at different times of the day and night, to
occur between 2230 and 0330 h (Schaefer, 1996). From a large-scale study of
spawning behavior of T albacares in the eastern Pacific it was reported that
spawning occurs almost entirely at night, between approximately 2200 and 0600 h
(Schaefer, 1998).
It appears that subsurface longline-caught female T albacares have signifi-
cantly lower gonad indexes than do purse-seine-caught female 7: albacares of the
same sizes caught in the same area-time strata in the eastern and western Pacific
(Suzuki et al., 1978; Koido and Suzuki, 1989; Bayliff, 1994). It seems likely that
these differences reflect behavioral differences in reproductively active and inac-
tive T. albacares. These differences suggest that mature, but reproductively in-
active, T. albacares seldom inhabit the near-surface warmer waters of the mixed
layer, where they would be vulnerable to capture by purse-seine gear. The spawn-
ing time during 1992 for a group of 3- and 6-year-old captive i? albacares held in
sea pens at the Yaeyama Station, Ishigaki, Japan, of the Japan Sea Farming Asso-
ciation (JASFA), was between 2000 and 0800 h, but mostly between 2000 to
2400 h (Masuma et al., 1993). During 1993 at the Yaeyama Station, the courtship
behavior of 3-, 4-, and 7-year-old T albacares in the same sea pen would normally
consist of similar-size males and females chasing one another. Commonly more
than one male was observed to be chasing after the same female, and the males
but not the females were identified as displaying body stripes during this period
(S. Masuma, JASFA, personal communication).
A population of 44 7: albacares held in a large (17-m-diameter, 6-m-depth,
1,36 1,900-liter) concrete in-ground tank at the Inter-American Tropical Tuna
Commission’s (IATTC) Achotines Laboratory in Panama first spawned in Otto-

ber 1996 (Bayliff, 1998). The initial spawning involved only two or three pairs ot
the largest fish (>90 cm in length). Each spawning event occurred around sunset,
and was preceded by courtship behavior during the late afternoon. The courtship
behavior included pairing of individuals, chasing, rapid color flashes exhibited by
individual fish, and rapid horizontal or vertical swimming. During the following
3 months of 1996 spawning was continuous, with many of the fish exhibiting
courtship behavior prior to each spawning event, which generally occurred be-
tween 1700 and 2000 h at water temperatures from 26.7 to 28.O”C. Behavioral
sequences associated with courtship become more pronounced and at higher fre-
quency approaching time of fertilization (V. Scholey, IATTC, personal communi-
cation). During most of 1997 spawning continued at nearly daily intervals in water
temperatures from 24.4 to 29S”C. Spawning ceased during the upwelling period
(mid-March to mid-April) when water temperatures ranged from 20.0 to 24.O”C.
Davis et al. (1998) has shown that size partitioning by depth occurs in 77z~-
rzus macco~ii in their spawning area. The smaller fish are more abundant in the
catches by deep longline gear and the larger fish are more abundant in catches of
shallow gear. This size partitioning by depth is apparently related to spawning
activity, with spawning fish being at the surface and nonspawning fish being
deeper. As fish get larger they spend proportionally more time spawning while on
the spawning ground.
The spawning time during 1998 and 1999 of‘ Thunnus orientalis broodstock
held at the Amami Station, JASFA, Japan, was between 1900 and 2300 h. The
observed courtship behavior is apparently similar to that for captive 7: allxzc~ares.
with more than one male commonly chasing after the same female and body
stripes and/or darker coloration displayed by the males during this period (S. Ma-
suma, JASFA, personal communication).
Katsuwonus pelamis captured at sea and placed in land-based tanks at the
Kewalo Research Facility of the National Marine Fisheries Service, Honolulu,
Hawaii, have spontaneously spawned about 8 h after capture at about 2400 h at
water temperatures of 23 to 24°C. However, spawning does not continue. prob-
ably due to the stress of captivity, and atresia of yolked oocytes within ovaries is
observed within 24 h. The spawning around 2400 h by captive K. yelumis appears
to be close to the time of natural spawning, on the basis of histological examina-
tions of skipjack ovaries (Hunter et al., 1986).
Euthynnus lineatus held in a 6.4-m-diameter. 37,000-liter tank at the IATTC’s
Achotines Laboratory in Panama spawned nearly continuously during 1994, with
the majority of the spawning occurring between approximately 2000 and 2400 h
(Bayliff, 1995). Spawning occurred in water temperatures of 25 to 28”C, and
when the temperature of the water in the tank decreased to less than 25°C the fish
stopped spawning.
Magnuson and Prescott (1966) observed Surda clziliensis in captivity to
exhibit courting and pairing behavior in a sequence previous to the simultaneous

and adjacent release of gametes while swimming in a circular path. There are some
reported observations of courtship behavior, consisting of pairing, chasing, and
wobbling, and lateral body markings and coloration changes in scombrids such as
Euthynnus lineatus (Hunter and Mitchell, 1967) and K. pelamis (Iverson et al.,
1970) in the ocean during daylight hours. This courtship behavior, particularly in
the later part of the day, although rarely observed in the field, appears to be normal
in scombrids, but does not indicate that spawning is occurring at exactly that time.
Investigations of courtship behavior and spawning in captive tunas through
assessing the roles of visual, acoustic, and chemical signals should be undertaken
in attempts to truly understand the act of spawning in tunas.
VI. SPAWNING FREQUENCY
Being multiple spawners, tunas, like many subtropical and tropical pelagic
fishes, continuously produce batches of hydrated oocytes which are released into
the sea in separate spawning events (Hunter et al., 1985). The estimation of
spawning frequency, as the mean spawning interval between sequential spawning
events, is essential for a comprehensive understanding of the reproductive biology
of tunas. Previously it was assumed, based on the number of modes present in
oocyte size frequency distributions, that almost all tunas, including Thunnus al-
bacares and Katsuwonus pelamis, spawn more than once during a spawning sea-
son, but not more than a few times (Bayliff, 1980; Matsumoto et al., 1984).
Knowledge of the appearance and longevity of postovulatory follicles in ova-
ries of tunas after spawning is necessary for estimation of spawning frequency
(Hunter et al., 1985, 1986; Schaefer, 1996). The age and longevity of postovula-
tory follicles have been determined only for K. pelamis (Hunter et al., 1986) and
7: albacares (Schaefer, 1996). More thorough validation of postovulatory degen-
eration and longevity is desirable, especially in species of tunas for which this has
not been investigated. However, the frequency of ovaries of mature females con-
taining postovulatory follicles has been used to estimate spawning frequency
(Table II) in K. pelamis (Hunter et al., 1986), T. albacares (McPherson, 1991;
Schaefer, 1996, 1998), Thunnus obesus (Nikaido et al., 1991), and Thunnus mac-
coyii (Farley and Davis, 1998). Schaefer (1998) estimated the fraction of mature
females in the population spawning per day to be 0.66, which is equivalent to a
spawning frequency of 1.52 days. This is a mean spawning interval for the average
mature female in the population during the 2-year period of that study, and does
not imply that individual fish are spawning at this rate throughout the year. In that
study the ovaries of 81% of the 565 females collected with migratory-nucleus or
hydrated oocytes (evidence of spawning within a few hours) also had post-
ovulatory follicles present (evidence of spawning within 24 h), which is equiva-
6. REPRODUCTIVE BIOLOG\r ,245
Table II
Estimates of Spawning Frequency (Mean Spawning Interval) for Female Tuna\
Species Days .4rea Reference
Katsuwonus pelamis 1.18 Western Pacific Hunter et rrl. ( 1YX6)

Thunnus albacares I .53 Western Pacific McPherson ( I YY I )
Thunnus albacares 1.52 Easrern Pacitic Schaefer ( I YYX)
Thunnus maccoyii I .62 Eastern Indian Farley and Davi\ (109X)
Thunnus obesus I .09 Western Pacilic Nikaido et cl/. (lYY1 i
lent to a spawning frequency of 1.23 days. This implies that reproductively active
7: albacares spawn almost daily. Similar spawning frequencies have been reported
for mature and reproductively active female T maccoyii, ?: obesus, and K. pe-
lamis, as indicated from the values in Table II. The incidence of both postovula-
tory follicles and late-stage oocytes indicates daily spawning in tunas (Figure 5).
This high frequency of spawning implies that in a reproductively active female
there is a continuous maturation of oocytes, which are recruited from the reservoir
of primary oocytes.
In the section on spawning behavior it was reported that there are apparent
behavioral differences in reproductively active and inactive 7: albacares, as indi-
cated from sampling of specimens from purse-seine and subsurface longline
gears. A recent study (Itano, 2000) of the reproductive biology of 7: albacares
in the central and western Pacific, using histological criteria, confirmed spawn-
ing throughout the year within 10” of the equator at a spawning frequency of
1.99 days, based on 5270 mature females sampled from purse-seine and subsur-
face longline gears. The spawning frequency for purse-seine samples was higher
(1.7 1 days) than that for longline samples (2.29 days), verifying the earlier obser-
vations. This disparity was more pronounced when examined from different set
types for both gears. The mean spawning interval for mature 7: ulhacares taken
by purse seines on actively feeding schools was 1.47 days, compared to 2.68 days
for samples taken from deep-set longline gear, which targets large tunas that are
spread out over large distances.
For the studies on spawning frequency of 7: ol?esus (Nikaido et al., 199 I ) and
7: maccoyii (Farley and Davis. 199X! the assumption is made that the postovula-
tory follicles probably do not persist and are not detectable for more than 24 h.
This is a reasonable assumption based on the results of the validation studies for
K. pelamis (Hunter et al., 19X6) and 7: albucares (Schaefer, 1996) which spawn
in similar sea-surface temperatures (~24°C) to those of 7: obesus and T maccoyii.
The rates of postovulatory follicle degeneration and resorption, along with oocyte
development, are more rapid in tunas than in fish inhabiting cooler waters, and are
Fig. 5. Migratory-nucleus or hydrated-stage oocytes and postovulatory follicles (p) in advanced
stages of degeneration, in five species of tuna. (A) Katswonus pelamis (X 25). (B) Thunnus albacares
(X40). (C) Thunnus maccoyii (X40). Microscopic slide from J. Farley, CSIRO, Hobart, Australia.
(D) 7%unnus obesus (X25). Microscopic slide from H. Nikaido, JASFA, Obama Fukui, Japan.
(E) Thunnus orientalis (X40). Microscopic slide from S. Tsuji, NRIFSF, Shimizu. Japan.
apparently correlated with temperature (Fitzhugh and Hettler, 1995). For chub
mackerel, Scomber juponicus, held at 20°C in the laboratory, postovulatory fol-
licles persisted in the ovary, and were detectable for up to 48 h after spawning
(Dickerson et al., 1992). The spawning frequency for S.juponicus in the Southern
California Bight during April-July at sea-surface temperatures presumably less
Fig. 6. Relationship between fraction of mature Z%umus albacares females spawning per day
and length. The circles are for .5-cm-length intervals. (From Schaefer, 1998.)
than or close to 20°C was 10.9 days (Dickerson et al., 1992). The spawning fre-
quency for S.juponicus around the Izu Islands, Japan, in sea-surface temperatures
of 16.5 to 18.8”C during April to June was 5.7 days during a period of 36 days.
Clarke (1987) showed that the Hawaiian anchovy (Encrusicholina purpurea)
spawns at intervals of about 2 days, as compared with about 7 days for north-
ern anchovy (Engruufis mordar), a cooler-water species (Hunter and Goldberg,
1980). The postovulatory follicle can be detected in E. mordax for just under 48 h
(Hunter and Goldberg, 1980), whereas for E. purpurea that period is apparently
no more than 24 h.
The relationship between length and the fraction of mature ZYalbucares fe-
males spawning is illustrated in Figure 6. The minimum observed length of I: alba-
cares at which postovulatory follicles were observed was 60 cm. From that length
there is a fairly rapid increase in the fraction spawning per day up to the estimated
length at which 50% of the females are mature (92 cm), where the predicted frac-
tion of mature females spawning per day is 0.61. The curve for the relationship
slowly approaches the asymptote following that point, and 7 1% of the females are
predicted to be spawning per day at 124 cm, the estimated length at which 90% of
the females are mature.
Davis et al. (1998) present data on the relationship between relative spawning
frequency and length for ?: mucco.yii. Spawning is first observed in the 150- to
159-cm length class, but is minor. From that length class there is a linear increase
in the fraction spawning per day to 0.38 in the 170- to 179-cm length class, 0.72
in the 190- to 199-cm length class, and 0.87 in the 200- to 209-cm length class,
the largest length class sampled, which is equivalent to a spawning frequency of
1.2 days. The findings from these two studies indicate the importance of estimat-
ing the relationship between spawning frequency and size class in tunas for inclu-
sion in algorithms of the estimation of reproductive potential of stocks.
An alternative method for measuring the spawning rate of tunas is based on
the frequency of ovaries containing hydrated oocytes (Hunter and Macewicz,
1985a). The incidence of mature female tunas with hydrated oocytes was used to
measure the rate of spawning by Schaefer (1987) for Euthynnus lineatus. The
frequency of occurrence of female E. lineatus throughout the spawning season
with ovaries containing hydrated oocytes led Schaefer (1987) to conclude that the
average interval between spawnings of E. Zineatus in the eastern tropical Pacific
was 2.1 to 5.7 days, depending on the area. Based on the apparent lengths of the
spawning seasons within areas, the estimated number of batches of eggs spawned
during the year by E. lineatus was 43 to 58. Studies at the IATTC Achotines
Laboratory, Panama, during 1994, when spawning of E. lineatus was nearly con-
tinuous, indicated that a group of eight fish averaging 50 cm in length spawned at
intervals of 1 to 5 days (Bayliff, 1995).
In females captured by longline gear in the Atlantic throughout the spawning
seasons during 1966 to 1990, the frequency of occurrence of ovaries containing
hydrated oocytes led Batalyants (1992) to conclude that the average interval be-
tween spawnings was 2.2 to 2.8 days for iT albacares and 1.6 to 3.1 days for
T. obesus. The hydrated oocyte method has the potential for obtaining reliable
estimates of the spawning frequency of tunas. However, the preferred method
should be the histological identification of postovulatory follicles in freshly fixed
ovarian tissues. This is because of the limited time period in which hydrated
oocytes are present in tuna ovaries, previous to spawning, and thus the limited
time period from which useful samples can be obtained, relative to the merits of
the alternative procedure (Hunter and Macewicz, 1985a; Hunter et al., 1986;
Schaefer, 1998).
Structural changes over seasonal cycles have been described from histological
examinations of teleost testes (Grier, 198 1), but there has been almost no research
on die1 testicular changes in relation to rhythmic spawning activity. Information
on testicular histology in tunas is scarce because most researchers have been sat-
isfied with gross morphological or gonosomatic indexes to measure reproductive
activity of males. Histological examinations of the testes from Thunnus alalunga
(Ratty et al., 1990) and T. obesus (Nikaido et al., 1991) have provided descriptions
of some aspects of spermatogenesis and characteristics of sexual maturity in male
tunas. An investigation of histological characteristics of testicular tissues from
reproductively active ZYalbacares provided criteria on the structural characteris-
tics of the vas deferens useful for estimation of spawning frequency and reproduc-
tive effort of males (Schaefer, 1996). Structural characteristics of the vas deferens.
specifically the amount of sperm present, its shape, and the staining of the epithe-
lium, are useful for detecting whether a male 1: albacares has recently spawned.
Utilizing these criteria for the combined samples from a 2-year study period of 7:
albacares in the eastern Pacific, the fraction of mature active males classified as
spawning was 0.97, equivalent to a mean spawning interval of I .03 days. The main
limitation to the technique is that spawning cannot be detected more than 12 h
after it occurs. Because 7: albucares are normally captured during daylight hours
in the purse-seine fishery in the eastern Pacific, spawning frequency estimates
from males could be determined only for fish caught during the relatively short
time between about 0600 and 1200 h. Spawning frequency estimates for tunas are
thus better estimated from the presence of postovulatory follicles that are detect-
able in ovaries from fish captured throughout the entire day, with the assumption
that the males spawn at similar times.
VII. FECUNDITY
The fecundity of tunas. like those of other multiple-spawning fishes, is not

fixed at the beginning of their spawning period. Their annual fecundity is indeter-
minate because tunas spawn numerous times during a season or year, and their
potential annual fecundity exceeds the number of oocytes within the ovaries at
any given time (Hunter et al., 1985). Annual fecundity can be estimated from
batch fecundity (the number of oocytes released per spawning) and spawning fre-
quency. However, only at the final stages of oocyte maturation, beginning with the
migratory-nucleus phase and followed by hydration, is there a distinct hiatus in
the distribution of oocytes from which the batch fecundity estimates can be de-
rived. This method is essential for accurate estimation of batch fecundity in mul-
tiple spawners. such as tunas, because only in this developmental stage of oogene-
sis can unequivocal counts of oocytes in samples from the spawning batch be
obtained. Unfortunately, most batch fecundity estimates on tunas and many other
multiple-spawning fishes have been based upon counts of oocytes which had not
entered their final stages of maturation and from ovarian tissue samples which had
been placed in Gilson’s fluid. This technique creates a further potential bias in
batch fecundity estimates because Gilson’s fluid causes significant shrinkage of
oocytes and compaction of the oocyte size distribution, which then complicates
partitioning of the most advanced group of oocytes from the adjacent group of
smaller oocytes.
Migratory-nucleus and hydrated oocytes can be easily distinguished from
other oocytes in ovaries of tunas by their larger size (~0.75 mm) and by their
appearance (Hunter et al., 1985; Schaefer, 1998). However, there is only a short
period from late afternoon until about 2200 h (previous to spawning) when ovaries
with migratory-nucleus or hydrated oocytes are found in Thunnus albacares

(Schaefer, 1996, 1998). The batch fecundity should be considered to be the num-
ber of migratory-nucleus or hydrated oocytes in the ovary (Hunter et al., 1985).
For each female, counts should be made of migratory-nucleus or hydrated oocytes
in a minimum of two subsamples of about 0.05 g each weighed to the nearest
0.1 mg (Schaefer, 1998). Ovaries should not be used for batch fecundity estima-
tion when postovulatory follicles 512 h age are identified through histological
examination, or loose hydrated oocytes are observed in the lumen of the ovary.
Each of the two subsamples yields an estimate of batch fecundity for each female,
calculated from the product of the number of migratory-nucleus or hydrated
oocytes per unit weight of the subsample and the total weight of the ovaries. The
mean of these two estimates provides the batch fecundity estimate for each fish.
Estimated mean relative batch fecundities for tunas, based on counts of dis-
tinct advanced stages of oocytes, are given in Table III. The relative fecundity es-
timates in Table III for I: albacares (67 oocytes/g body weight) and Thunnus
maccoyii (57 oocytes/g body weight) are similar, but considerably greater than the
estimate for Thunnus obesus (31 oocytes/g body weight), and considerably less
than the estimates for Katsuwonuspelamis (82 oocytes/g body weight) and Euthyn-
nus line&us (99-136 oocytes/g body weight). For temperate scombrids, the esti-
mated batch fecundities, based on migratory-nucleus or hydrated oocyte counts,
were 168 oocytes/g body weight (Dickerson et al., 1992) and 158 oocytes/g body
weight (Yamada et al., 1998) for Scomberjaponicus, and only 28 to 55 oocyteslg
body weight for Somber scombrus (Alheit et al., 1987; Watson et al., 1992). In
other studies of tunas in which batch fecundity determinations were made using
advanced yolked oocytes which were not yet in the final stages of oogenesis, or
tissues were subjected to treatment with Gilson’s fluid, the estimates should be
considered as biased substantially upward.
Hunter et al. (1985) demonstrated that the minimum number of females re-
quired for an appropriate estimate of the batch fecundity for northern anchovy,
Engraulis mordax, was 50. The estimate for T. albacares (Schaefer, 1998) is based
TableIII
Estimates of the Relative Batch Fecundity (Oocytes per Gram of Body Weight) of Tunas
Species Fecundity Area Reference
Euthynnus linearus 99-136 Eastern Pacific Schaefer (1987)

Karsuwonus pelamis 82 Western Atlantic Goldberg and Au (1986)
Thunnus albacares 67 Eastern Pacific Schaefer (1998)
Thunnus maccoyii 57 Eastern Indian Farley and Davis (1998)
Thunnus obesus 31 Western Pacific Nikaido et al. ( 199 1)
on a sample size of 345 females, but all of the other estimates given in Table 111
are based on inadequate sample sizes, Obtaining females in advanced stages of
oogenesis, containing migratory-nucleus or hydrated oocytes, can be difficult. The
time period when ovaries are in this developmental stage is only a few hours and
availability of samples is normally restricted to the periods of commercial fishing
operations, which do not necessarily coincide with the period just previous to
spawning. In addition to the importance of appropriate sample sizes in estimation
of batch fecundity, there are other sampling considerations. These include, but are
not limited to, the length distribution of samples from throughout the size range
of reproductively active females and suitable geographic and temporal coverage
for the stock under investigation (Hunter et al., 1985, 1992; Schaefer, 1998).
Batch fecundity increases with body length for the species listed in Table III
(Figure 7). Although not illustrated in Figure 7, the data for each of these species
clearly indicate the high variation in batch fecundity estimates among tunas of
similar size. For 7: ulhacares, for example, the estimates of relative fecundity
ranged from 4.9 oocytes per gram of body weight for a 118-cm fish to 174.0
oocytes per gram of body weight for a 126-cm fish. Although the relationship
between batch fecundity and length is expected to be curvilinear, and linear be-
tween batch fecundity and weight (Hunter et al., 1985, 1992; Schaefer, 1998), it
is analytically possible for the batch fecundity in tunas to be linearly dependent
on both weight and length (Schaefer, 1987).
Interannual and geographic variation in batch fecundity estimates has been
reported for tunas. Even with the high variability in batch fecundity estimates of
fish of the same size, statistical comparisons have indicted significant differences.
For example, the predicted batch fecundity estimate for a 125-cm Z alhucureLs
was 1.454 million oocytes one year, and 2.495 million oocytes the next, within
the same area of the eastern Pacific (Schaefer, 1998). The information on annual
variation in batch fecundity for marine fish, especially tunas, is very limited be-
cause in most instances batch fecundity and other reproductive characteristics are
derived from a single year of sampling. For Engmulis tnordax, whose reproduc-
tive biology has been investigated extensively, significant interannual variation in
batch fecundity has been observed, the average number of eggs produced per
spawning by a standard female varying by a factor of 2 (Hunter et al., 1985).
Temporal variation in batch fecundity estimates may be associated with factors
such as temperature and prey availability (Wootton, 1982), although there is little
empirical evidence for either in the literature pertaining to pelagic marine species
sampled in the field. Geographic variation was also observed in batch fecundity
estimates for ‘T:ulbacures, with the greatest predicted estimates of batch fecundity
in the most northern area in the eastern Pacific (Schaefer, 1998). The batch fe-
cundity of Euthynnus lineutus was also shown to increase with latitude in the
eastern Pacific (Schaefer, 1987). Geographic variation in fecundity has been re-
ported for several species of fish. with greater fecundities commonly found at
higher latitudes. The batch fecundity of Engraulis mordax off Oregon is signifi-
cantly greater than for those off California (Hunter and Goldberg, 1980; Laroche
and Richardson, 1980). Geographic differences in batch fecundity and length at
sexual maturity of tunas suggest a lack of complete mixing of fish among areas.
These differences appear to reflect genetic variation, although environmental ef-
fects also may be partly responsible.
Batch fecundity has also been reported to vary significantly during the spawn-
ing season in many fish species (Conover, 1985). A decrease in batch fecundity
was reported for S. scombrus during the spawning season in the Atlantic as indi-
viduals moved northward (Watson et al., 1992). Batch fecundity has been shown
to depend upon rations in several laboratory studies of nonscombrids (Wootton,
1979) and probably depends on environmental factors of the habitat of fishes as
well (Wootton, 1982). Female haddock, Melanogrammus aeglejinus, which is a
multiple spawner, produced fewer eggs at successive spawnings when fed at main-
tenance rations rather than at high rations (Hislop et al., 1978).
As mentioned before, the annual fecundity is the product of the spawning
frequency and the batch fecundity. The annual relative batch fecundity (number
of oocyteslg body weight/year) was estimated to be 14,141 and 17,280 for the
average 2- and 3-year-old T. albacares, respectively, in the eastern Pacific (Schae-
fer, 1998). These estimates illustrate that the annual egg production is far greater
for the average 3-year-old than for the average 2-year-old. Predictive models for
length at maturity and spawning frequency should be coupled with those for batch
fecundity and used with abundance estimates for females to produce estimates of
the potential annual egg production of tuna stocks.
VIII. SEX RATIOS
Tunas display no sexual dimorphism in either external morphological charac-

ters or color pattern (Bayliff, 1980; Collette and Nauen, 1983). In a recent com-
parative study of morphological features of thawed Thunnus albacares and Thun-
nus obesus it was not possible to distinguish males from females by any of the
external characters quantitatively evaluated (Schaefer, 1999). Aside from the pre-
viously mentioned rare instances of hermaphroditism reported in Katsuwonus
pelamis (Raju, 1960; Uchida, 1961), tunas are heterosexual.
Sex ratios reported in most studies on tunas are based on gross examinations
of the gonads of individuals from commercial landings. The discrimination of
ovaries versus testes, from gross examinations, is problematic in the smaller in-
dividuals with undeveloped gonads. In early studies on reproductive biology of
K. pelamis and 7: albacares in the eastern Pacific (Schaefer and Orange, 1956;
Orange, 1961), and a later study addressing sexual dimorphism in growth (Wild,
1986) the inability to assign sex to smaller specimens is apparent from the clas-
A
0.2 -
0.4
0.3
O.l- - // -
0
35 40 45 50 55 60 65 70
0.8
jlj /
‘45 ,
50 I
55 60I 65I 70I 75
5
D
4-
3-
2-
1 -
//,
0
100 120 140 160 180 200
9
-E
6
3
/
0
150 160 170 180 190 200
Fig. 7. Relationships between hatch l&undity and length. (A) Eurth.vnnus linrum.\ (Schaefer
987). (B) Karsuwonus pelumis (Goldberg and Au. 1986). (C) Thunnus trlhuctrrrs (Schaefer. 199X)
D) Thunnus O~PSUS (Nikaido et c/l., 1991 ). ( F.) 7humrct mcrc~~ovir (Farley and Davis, 1998).
sification of individuals as of indeterminate sex. There are numerous instances in

the literature where the sex ratios reported for the smaller fish, especially below
lengths at 50% maturity, should be considered suspect when sex identifications
were based solely on gross examinations. Criteria developed through microscopic
examinations of gonadal tissues for the separation of undeveloped ovaries and
testes through gross examinations are practical only down to a limited range in
length. It is preferable to obtain positive identifications of sex for smaller fish with
undeveloped gonads from microscopic examinations of gonadal tissues. Immu-
nochemical sex discrimination of live r albacares has been conducted (Takemura
and Oka, 1998), but the lower size limit for sex discrimination has not been deter-
mined. Also, that technique would appear to be most promising for sex discrimi-
nation of tunas being held as experimental broodstock.
The overall sex ratios reported for most tuna species, when adequately sam-
pled, do not deviate significantly from the expected 1 : 1 ratio. However, a pre-
ponderance of males in the larger length classes has been reported for several
tuna species investigated: Euthynnus afinis (Yesaki, 1994a), Euthynnus lineatus
(Schaefer, 1987), Thunnus alulunga (Otsu and Sumida, 1968), 7: ulbacures (Su-
zuki, 1994; Wild, 1994; Schaefer, 1998), Thunnus muccoyii (Caton, 1991), 7: obe-
sus (Miyabe and Bayliff, 1998; Pallares et al., 1998), and 7: thynnus (Clay, 1991).
This is most interesting, since for most fishes it is the females which attain the
largest sizes and are predominant in the larger length classes (Pauly, 1994). The
differentials in sex ratio within size classes of tunas have been suggested to be due
to differences between males and females with respect to growth, mortality, or
availability. The almost complete absence of females within the larger size classes
of tunas seems to be caused by differential natural mortality rather than differen-
tial growth or vulnerability to capture (Schaefer, 1998).
For 7: ulbucures, a significant deviation from the expected 1: 1 sex ratio in the
50- to 54.9-cm class (41.9% males) was observed, based on sex identifications
through histological examinations of gonadal tissues (Schaefer, 1998). The pre-
ponderance of females in this length interval may be related to differences in
growth rates between the sexes, but there is no empirical evidence to support that
hypothesis at this time. A higher proportion of females in the smaller length
classes has also been reported in other species of tunas, such as K, pelumis (Ma-
tsumoto et al., 1984), but the determinations of sex in those studies were not based
on histology, and the results should thus be considered dubious.
Most sex ratio data for tunas is reported as a by-product of investigations of
spawning distributions, maturation, and fecundity and have not been particularly
useful for investigating specific hypotheses. Investigations of sex ratio variation
within schools, geographically, seasonally, and relative to reproductive activity
require proper experimental designs, including adequate sample sizes and, most
importantly, accurate determinations of sex. Analyses of sex ratios within schools
of 7: albacures appear to indicate that a significant factor in the observed sex ratio
6. REPRODUCTIVE BIOLOGY 25-4
is the presence of reproductively active females. There may be some segregat~ori

of tuna schools by sex and/or a higher proportion of males within schools wtth
reproductively active females present. However. data sets obtained thus liu arc
insufficient for resolution of these questions. Significant deviations from an ex-
petted 1 : 1 sex ratio within schools of Engraulis mot&x have been attributed to
behavioral factors such as spawning aggregations (Klingbeil, 1978). Schaefer
(1998) indicates the importance of sample sizes in excess of 100 individual.\ pet
school in order to test such hypotheses. There is obviously a need to investigate
further various aspects of differential sex ratios in tunas.
IX. REPRODUCTIVE ENERGETICS
The environmental temperature of tunas undoubtedly acts upon the reproduc-

tive system through the total metabolic rate. Temperature is a controlling factor in
physiological processes, and tunas. which have high metabolic rates, have evolved
to maximize reproductive success within their habitat (Brill, 1996). Tunas re-
produce in regions of near-maximum sea-surface temperatures, permitting high
spawning rates, reproductive output, and growth of their offspring.
There is very little information on the energetic costs of reproduction in tunas.
Studies on other families of marine and freshwater fishes suggest, however, that
the energetic costs associated with reproduction are significant, and can have im-
portant consequences affecting growth and mortality rates after sexual maturation
(Wootton, 1990). Estimates of energetic costs for reproduction in tunas can be
evaluated from a bioenergetics approach (Calow, 1985: Wootton, 1985). A bio-
energetics approach to an evaluation of reproductive costs involves the use of an
energy budget equation to account for energy gains, losses, and transfer within
the organism. The equation for an energy budget follows the general form (Job-
ling, 1994)
R = f‘ t U + M 4~ P.
where R is the energy gained as food, F is the loss as feces, M is the energy cost
of metabolism, U is additional energy loss, and P is growth or energy storage. The
energy retained (P) can be differentiated as that of somatic growth (P,) or energy
channeled into reproductive growth (P,).
The energetic costs of spawning by female and male Thunnus albacares (ex-
cluding behavioral activities) have been estimated (Schaefer, 1996, 1998). The
energetic cost of spawning by the females is estimated by the product of relative
batch fecundity and oocyte weight. The relative batch fecundity for 7: cdbacarrs
is 67.3 oocytes per gram of body weight (Schaefer, 1998), and the mean wet
weight of a 7: albacares oocyte in the migratory-nucleus stage, just before the
hydration process begins. was estimated to be 0.157 mg (Schaefer, 1996). The
costs of a single spawning, the average daily cost, and that of the annual egg
production are estimated to be 1.06, 0.7, and 254% of the body weight for the
average female. The energetic cost of spawning by the males is estimated by sub-
tracting the percentage of calculated body weight of the testes just after spawning
from the percentage of body weight of the testes just before spawning occurs
(Schaefer, 1996). The costs of a single spawning, the average daily costs, and that
of the annual sperm production are estimated to be 0.34,0.33, and 120% of body
weight for the average male. Estimates of total daily and annual energy costs for
reproductively active 7: dbacares can be obtained from the bioenergetics ap-
proach. Olson and Boggs (1986) estimated a mean daily ration of 5.2% body
weight from a bioenergetics model incorporating energy expenditures for loco-
motion, metabolism, energy losses, and growth. The estimated mean energy ex-
penditure for growth was about 0.41% of body weight per day. If the estimated
daily cost of spawning for a female of about 0.7% of body weight per day is
adjusted to account for waste losses, as in Olson and Boggs (1986) when added
to the overall bioenergetics estimate a daily ration estimate of about 6.3% of body
weight is obtained for total energy expenditure. The estimated daily ration to ac-
count for total energy expenditure in reproductively active males is 5.7% of body
weight. The annual investments of energy in reproduction as a proportion of total
energy is then estimated to be about 17.5 and 8.8% for the average reproductively
active female and male, respectively. In comparison, the annual investment of en-
ergy in growth, from Olson and Boggs (1986), as a proportion of total energy is
estimated to be about 10 and 11% for females and males, respectively. These
estimates of the reproductive energetics of 7: albucures must be interpreted cau-
tiously. There are numerous assumptions and sources of imprecision in the pa-
rameter estimates to the model. These include the estimation of reproductive costs
for males and metabolic rates in Olson and Boggs (1986) which do not fully ac-
count for the expected differences between juveniles and adults.
Although the energetic investment in eggs is greater than that in sperm, the
energetic costs of engaging in reproductive behavior may be markedly higher for
the males, and the overall investment in reproduction may be similar for the two
sexes (Jobling, 1994). However, Wootton (1990) reports there to be no estimates
of energy costs of courtship available, and it seems unlikely that they are a signifi-
cant component of the energy budget. Wootton (1990) also states that, compared
with sperm, each egg which provides the yolk required for development of the
larvae to the point of being able to feed exogenously represents a massive cyto-
plasmic investment.
For Kutsuwonus pelumis, Hunter et al. (1986) estimated the cost of a single
spawning to be about 2% of the body weight. Based on an estimated spawning
frequency of 1.18 days, the daily cost of spawning a single batch of eggs would
be 1.7% of body weight per day. However, reproductive costs are probably over-
estimated because the relative batch fecundity estimate used 100 eggs per gram as
the estimated weight for a single egg. An estimate of the cost of a single spawning
of Euthynnus lineatus (Schaefer, 1987) was reported to be 1.77% of the body
weight. Based on an estimated spawning frequency of 2.1 to 5.7 days, the daily
cost of spawning a single batch of eggs would be 0.31 to 0.84% of body weight
per day. This estimate may also be biased because of the inherent problems in an
estimation of spawning frequency based on the occurrence of fish with hydrated
ovaries, as opposed to the postovulatory follicle method (Hunter and Macewicz,
1985a).
In northern anchovy, Engraulis mordax, the annual investment of energy in
reproduction is estimated to increase from 8% of the body weight for I- and
2-year-olds to 11% for 3- and 4-year-olds (Hunter and Leong, 1981). For female
pike, Esox Lucius, the annual investment of energy in reproduction increases from
0% of the body weight in the first year of life to 11 to 16% over the second, third,
and fourth years (Diana, 1983a). Diana (1983b) reports that 6 to 18 times as much
energy is deposited in the ovaries as in the testes. In males the annual allocation
of energy to reproduction increases from 0% of the body weight in the first year
of life to 4 to 5% in the second, third, and fourth years.
Somatic and gonadal growth can be considered to be in competition for lim-
ited resources, and a decrease is commonly seen in somatic growth rate when fish
mature (Jobling, 1994). There are direct trade-offs between growth and reproduc-
tion, which are important components of fitness in fish, since energy channeled
into the gonads detracts from somatic growth, and hence future fecundity (Ware,
1982; Roff, 1983). For 7: ulbacares from the eastern Pacific the estimated lengths
at which 50% of the females and males were mature were 92 and 69 cm, respec-
tively (Schaefer, 1998). The potential advantage of males attaining sexual matu-
rity at lesser lengths than females and contributing to the population’s gene pool
earlier is that it could increase the overall fitness and reproductive success of the
population through exchange of genetic material among different age groups. An
investigation of growth of 1: albacures in the eastern Pacific based on otolith
increments revealed sexually dimorphic growth, with size at age showing that
young females are consistently larger than males of the same age. However, the
growth curves cross one another at about 95 cm (2.12 years), and thereafter the
males are larger than the females (Wild, 1986). It is possible that these differences
in growth pattern are also related to the higher energetic costs of spawning for
females. The inflection points in the nonlinear growth models fit to the separate
data for females and males were at approximately 1.4 and 1.6 years of age, after
which the growth rates begin to slow down. The approximate ages for the lengths
at 50% maturity for females and males are estimated to be about 2.0 and 1.5 years
of age. These results appear to indicate that the available energy for growth is
being allocated toward gonadal development and maturation, and there is a poten-
tial decrease in the available energy at this point to maintain the high rate of so-
matic growth observed during the juvenile stage. The relationships between age,
KURT M. SCHAEFER
/
// /I
80
t
/
70 /
,
60 t/ 1’
I 1 I
1.0 1.5 2.0 2.5 3.0

AGE IN YEARS
Fig. 8. Relationships for growth and maturation for female Thunnus albacares from the eastern
Pacific. The growth schedule (solid line) is derived from the predictive function for age at length from
Wild (1986), and the maturity schedule (broken line) is derived from predicting age at length, from
Wild (1986), for the proportions mature at length from Schaefer (1998).
growth, and maturation in female 7: albacares are illustrated in Figure 8. The

minimum age at maturity in females is about 1.5 years of age, with 80% of the
fish mature by about 2.5 years of age, and thus the onset of maturity occurs over
a l-year age span.
Because body size is an important determinant of both maturity and fecundity,
variability in growth has potentially important consequences for the estimation of
the productivity of the population. A common response to an increase in growth
rate of fish is a decrease in the age of maturity. This is sometimes, but not al-
ways, accompanied by a change in the size at which the fish reaches sexual ma-
turity (Wootton, 1990). Additional research to evaluate relationships between age,
growth, and maturation in T. albacares has been conducted (Schaefer, 1998). The
investigation consisted of examining geographic variation in growth and matura-
tion of 7: albucares in the eastern Pacific. The growth rate for the fish from the
southern area are apparently greater than that for those from the northern area
(where sea-surface temperatures are significantly cooler) until the fish are just
under 3 years of age, at which time it decreases. Earlier onset of maturation was
observed in the southern area. Differences in maturity appear to be expressed
largely as shifts in the maturity schedule along the length axis, rather than as
changes in the shape of the curves once maturation is initiated. For each propor-
tion mature (0.25,0.50, and 0.75) the southern fish were shorter and younger than
the northern fish. One of the energetic implications of these results for 7: alhcr-
cares is the fact that the analysis indicates that for the fish of the southern group,
which have an earlier age at maturity, there is a decrease in the rate of growth.
relative to the northern group, less than 1 year after maturation. This is as expected
from energy allocation models of growth and reproduction in fish (Roff, 19X3).
Reproductive tactics of tunas are, no doubt, determined by the trade-offs between
growth and reproduction. There may also be a decrease in survival associated with
reproduction. However, in order to assesshow growth and reproduction contribute
to fitness in tunas it is necessary to know precisely the age- or size-dependent
mortality functions (Roff. 1983), which are not available.
Aside from the cost of reproduction leading to an apparent decrease in growth,
other costs of reproduction may include increases in mortality, or decreases in
future fecundity (Wootton, 1990). The higher natural mortality rate for female
7: ahcares above 135 cm may be due to the much higher estimated energetic
costs of spawning for females (0.7% of body weight/day) than for males (0.33%
of body weight/day; Schaefer, 1996), and possibly to aggressive reproductive be-
havior of the males causing injuries to females before and during spawning events.
Ware ( 1984) reports that several theoretical studies for iteroparous fishes demon-
strate a link between reproduction and mortality, as both rates often increase with
body weight and age during the later stages of the life cycle. Several theoretical
studies on the energetic costs of reproductive effort for fish other than tunas have
been conducted, but empirical studies are scarce. In laboratory experiments on the
Japanese medaka, Olyzias lutipes, which spawns daily, Hirschfield ( 1980) found
mortality of females to be greatest at high levels of reproductive effort and tem-
perature. The fish with higher reproductive effort lost more body weight, which
reportedly led to mortality. Hirschfield also stated that individual fish may allocate
insufficient energy to maintenance costs while reproductively active, even at the
cost of an increased likelihood of mortality. Anderson and Ursin ( 1977) and
Laevastu and Larkins (198 1) have pointed out that spawning stress mortality may
be a significant portion of senescent mortality in all fish. Pauly (1994). however,
suggests that the “reproductive drain hypothesis” should be refuted for fishes in
general; when considering the evidence for tunas, his arguments do not appear
justified.
In mature marine species, reproductive growth will apparently continue to the
detriment of somatic growth, but when food supplies are limited the reproductive
growth will cease and atresia of yolked oocytes occurs. It appears that the greatest
effect of food limitation on reproductive effort is a decrease in fecundity, which
has been demonstrated in a number of fishes. For 7: alhucures no significant re-
lationship was observed between relative fecundity and body weight, and it thus
does not appear that larger females allocate relatively more energy to batch fe-
cundities than do smaller females. The average percent body weight for ovaries
containing hydrated oocytes was 2.2% for a 90- to loo-cm female and 2.6% for a
140- to 150-cm female (Schaefer, 1998). Of the 345 females for which batch fe-
cundity estimates were derived in that study, only 22 had alpha atresia present in
the ovaries, but 18 of those, or 82%, had less-than-average batch fecundities. The
process of atresia in the ovary of tunas is most likely an indicator of the energy
reserves in somatic tissues in areas where sea-surface temperatures are consis-
tently above minimum spawning temperatures. In areas where sea-surface tem-
peratures fall below spawning temperatures, however, atresia most likely occurs
even when energy reserves remain at reasonable levels to support continued repro-
ductive activity. The low percentage, 7.5%, of reproductively active T. albacares
females with minor alpha atresia indicates the apparent rapid cessation of repro-
ductive activity once the process of atresia begins (Schaefer, 1998). However, in
Scomber japonicus, alpha atresia of the advanced yolked oocytes was common
throughout the spawning season-even early in the season with 12% of the fe-
males having high levels of alpha-stage atresia in their ovaries (Dickerson et al.,
1992).
Batch fecundity has been shown to depend upon ration in laboratory studies
(Wootton, 1979). Bagenal (1969) found that brown trout, Salmo trutta, at higher
rations contained significantly more eggs, but at a smaller size. Female haddock,
Melanogrammus aeglefinus, which is a multiple spawner, produced fewer eggs at
successive spawnings when fed at maintenance rations than did fish at high rations
(Hislop et al., 1978). Bagenal (1966) stated that populations of plaice which were
under the best condition had the highest fecundities. Research conducted on rates
of atresia based on starvation of captive Engraulis mordax, along with rates of
recommencement of spawning after resuming feeding (Hunter and Macewicz,
1985b), provides insight into relationships between feeding, somatic energy re-
serves, and egg production. Similar laboratory studies for tunas should be encour-
aged, and also sampling of tissues from wild tunas, to investigate relationships
between body composition and egg production. Controlled experimental studies
on the allocation of energy among maintenance, growth, and reproduction with
varying environmental conditions, including temperature and ration, would be
most informative. However, the results of such experiments would need to be
evaluated under natural conditions through field studies.
The apparent spawning strategy of tunas, which consists of spreading huge
quantities of eggs over enormous areas, either continuously or for prolonged pe-
riods in high temperatures, is obviously intended to minimize risk in a highly
variable and unpredictable environment (i.e., distributions of prey organisms and
predators). In comparison, the related Scomber spp. spawns on a more restricted
spatiotemporal scale within its habitat when seasonal zooplankton production is
highest and temperatures are on the increase (Lambert and Ware, 1984). In the
case of tunas. it appears that the limiting factor to maintain reproductive activity
is for the adults to locate and remain in areas of high concentrations of forage. In
contrast Scomber has opted to focus its strategy on expending its reproductive
energy seasonally, to potentially maximize survival of the larvae. In both species
the strategies have apparently evolved, within their respective habitats, to exploit
high temperatures which allow a high growth rate and optimize the chances for
the larvae to pass quickly through their respective predatory fields (Lambert and
Ware, 1984).
X. CONCLUDING REMARKS
Temperatures above 24°C appear to stimulate maturation and reproductive ac-

tivity in tunas. The time of spawning appears to be modified by environmental
temperature, with spawning of stocks occurring almost continuously in tropical
regions, but at phase in the more northern and southern hemispheres. Whereas
temperate marine pelagic fish release several successive batches of eggs over a
period of a few months, during predictably high planktonic production, most tunas
spawn batches at nearly daily intervals throughout most of the year and over ex-
tensive oceanic regions of highly unstable and fluctuating planktonic production.
It is the asynchronous oocyte development in ovaries of tunas which enables them
to employ the tactic of opportunistic oviposition.
The reproductive patterns of tunas are remarkably diverse, and their evolution-
ary basis involves the acquisition and allocation of energy resources to maintain
high rates of growth and reproduction to survive within the environmental con-
straints of their respective habitats. We see clearly the divergence in life histories
when focusing on the reproductive patterns and characteristics of two groups
within the tribe, Katsuwonus pelamis and Thunnus ulbacares versus Thunnus
maccoyii, Thunnus orientalis, and Thunnus thynnus. The members of the former
group are distributed widely, and spend their lives in tropical and subtropical wa-
ters, reaching sexual maturity within 1 to 2 years, and then spawning continuously
throughout the remaining few years of their lives. In contrast, members of the
latter group are also found in tropical and subtropical seas, but have evolved to
exploit highly productive temperate regions as well. They do not reach sexual
maturity until several years of age, demonstrate directed spawning migrations,
have restricted spatiotemporal spawning distributions, and may live for an addi-
tional 20 years after spawning.
A very limited amount of scientifically useful information is available on the
reproductive biology for most tunas. Spawning distributions, maturity and fecun-
dity schedules, and size-specific sex ratios have not been adequately investigated,
and these important reproductive parameters which should be incorporated into
statistical assessment models are essentially nonexistent. The greatest amount of
useful information presently exists for 7: albacares, 7: maccoyii, and K. pelamis,
although even for these species the information is not complete. With respect to
T. albacares and K. pelamis, parameters should be estimated for the stocks upon
which large-scale commercial fisheries operate within the three major ocean ba-
sins (Atlantic, Indian, and Pacific). Furthermore, the lack of useful scientific in-
formation on the reproductive biology for T. thynn~s in the Atlantic and Mediter-
ranean is perplexing when considering the historical existence, commercial value,
and management for this species.
The rational exploitation and responsible management of stocks of tunas are
dependent on the understanding of their biology. Precise knowledge of reproduc-
tive biology, growth, and mortality of tunas is essential to conduct proper assess-
ments. Studies focusing on the important reproductive parameters for stocks of
commercially valuable species of tunas are needed, but only if proper experimen-
tal designs and methodologies are employed. Furthermore, complementary stud-
ies on growth and reproductive biology of tunas should be encouraged in attempts
to elucidate these interdependent complex physiological processes which are the
basis for quantitative ecological evaluations of the reproductive potential of tuna
stocks.
ACKNOWLEDGMENTS
Thanks are extended to John R. Hunter and Beverly J. Macewicz for sharing their knowledge and
enthusiasm on the reproductive biology of fish. I gratefully acknowledge the reviews of drafts of the
manuscript by William H. Bayliff and two anonymous reviewers.
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7
MECHANICAL DESIGN FOR SWIMMING:

MUSCLE, TENDON, AND BONE
MARK W WESTNEAT
STEPHEN A. WAINWRIGHT
1. Introduction
II. External Morphology: Body Form and Fin Shape
III. Axial Muscle: Myomeres and Myosepta
IV. Axial Muscle: Red Muscle Morphology
V. Axial Connective Tissues: Main Horizontal Septum
VI. Muscle Function: Tendon Linkages in the Horizontal Septum
VII. Muscle Function: Principles of Hydrostatic Pressure
VIII. Mechanical Design of the Caudal Fin Muscles and Tendons
IX. The Backbone and Vertical Septum
X. Summary and Future Research
The muscle, tendon, and bone of tunas and mackerels form a mechanical sys-
tem specialized for both high-performance swimming and long-distance cruising.
The axial musculature, connective tissues, and skeleton of scombrid fishes exhibit
modifications of the basic actinopterygian design for swimming that highlight
mechanisms for the generation and transmission of force from muscle to caudal
fin. This chapter illustrates the axial morphology of scombrids and analyzes the
mechanics of thunniform locomotion. The external body shape and tail mor-
phology are described for a variety of scombrid fishes. We review the complex
shapes of myomeres and myosepta in the mackerels and tunas and reveal the ori-
entation of two major systems of collagen fibers in myosepta and horizontal septa
with respect to points of attachment to skeleton and skin. Locomotor muscle is
arranged in serially nested cones that are associated with complex arrays of con-
nective tissue. The collagen fibers of myosepta, horizontal septa, and skin are the
tensile elements that transfer locomotor forces from the contraction of myomeres
to the backbone and caudal fin during locomotion. Locomotor muscle pulls
against a three-dimensional structure of tendons, septa, and skin that is kept in
tension by the radial expansion of the contracting muscle. The main horizontal
271
TWIO : Volume 1Y Copyright 0 ZIH~I hy Academu Prcs\
FISH PHYSIOLOGY All uphts of reproductmn in any form resewed
272 MARK W. WESTNEAT AND STEPHEN A. WAINWRIGHT
septum is formed by the convergence of myosepta and is likely to be the major

transmitter of muscle force to the axial skeleton. The vertical septum is formed
from the serial neural spines and a fabric of collagen fibers connecting them. We
propose a biomechanical model for the function of the neural spines and vertical
septum in energy storage and return in scombrids. A posterior system of muscles
and tendons operates the lunate caudal fin in tunas and mackerels. A new me-
chanical model is proposed for the function of the caudal muscles in fine tuning
the shape and motion of the caudal fin. The construction of biomechanical models
allows the identification of several musculoskeletal mechanisms of locomotion in
scombrid fishes that direct future research on muscle function. Key features of the
locomotor design of tunas, mackerels, and outgroups are highlighted on a phy-
logeny to identify the major evolutionary stages in the functional morphology of
scombrid locomotion.
I. INTRODUCTION
The locomotor system of fishes has emerged as a primary focus for the study
of vertebrate biomechanics because investigators are combining studies of muscle
physiology, comparative morphology, hydrodynamics, and behavior to answer
central questions about the mechanics of swimming. The morphology of fish lo-
comotor systems plays a key role in our understanding of the mechanisms of pro-
pulsion in fishes. From body shape to the anatomy of fins, muscles, and vertebrae,
the mechanical design of fishes has generated many of the central hypotheses now
being tested in fish locomotion. This is particularly true for scombrid fishes
(mackerels, tunas, and relatives) with their streamlined bodies, propeller-like tails,
and the unique structure and function of tuna muscle and connective tissues. Thus,
this chapter presents the comparative morphology of tunas and their relatives from
the perspective of mechanical designs that contribute to swimming performance.
Tracing the evolution of key structural features on a phylogenetic hypothesis (Fig-
ure I) reveals several stages in the modification of the high-performance scom-
broid locomotor design.
All scombrid fishes swim by generating waves of undulation along the length
of the body and producing lateral thrusts of the tail. Studies of the kinematics of
mackerel indicate that mackerels swim by body undulation in which significant
body bending occurs. Tailbeat frequency is relatively high (up to 15 Hz), length-
specific wavelength is about 1.O, and wavelength is longer than stride length, the
distance traveled in one tailbeat cycle (Videler and Hess, 1984; Wardle and Vi-
deler, 1993). Tuna swimming is performed with tailbeat frequencies and ampli-
tude ranges that are similar to other scombrids, but with significantly longer pro-
pulsive wavelength and maximum stride length values (Dewar and Graham,
1994). These behavioral studies suggest that tunas are stiffer and bend their ver-
7. MECHANICAL DESIGN FOR SWIRIMING 27.3
Fig. 1. Phylogenetic hypothesis of relationships for some of the scombroid fishes for which we
have data on locomotor morphology. Changes in characters of locomotor structure and swimming
mode are indicated on the tree. Tree is for a subset of taxa reviewed by Collette ( 1997). (A) Charac-
teristics of most fishes: myomeres arranged m nested cones. slow oxidative red muscle laterally posi-
tioned, horizontal and vertical septa function as force transmission systems, and caudal tin forked or
paddle shaped. (B) Anterior-pointing cones (APCs) elongate, main horizontal septum (MHS) hyper-
trophied, great lateral tendon (GLT) hypertt-ophied, increase in aspect ratio (AR) of forked and lunate
tails, and caudal fin with rays modified as Raps. (C) Undulatory locomotion, highest AR caudal fins,
neural spines platelike. and extremely elongate muscle cones. (D) Carangiform locomotion, and neural
spines strongly curved posteriorly. (E) Thickened body, internalized red muscle, and reduction of
hypochordal longitudinalis (HL) muscle. (F, Thunniform locomotion, high-AR cat&al tin, fully inter-
nal red muscle. elongate APCs, endothermy. long. low-angled posterior oblique tendons, hypural plate
fused, caudal keel with joint, and HI- ligamcnton\.
tebral columns less than mackerels while attaining similar high-performance lo-
comotion. Biomechanical analyses indicate that scombrid locomotion depends
critically on the transmission of forces from locomotor muscle to the backbone
via connective tissues, including the myosepta, the horizontal and vertical septa,
and the skin (Wainwright, 1983; Westneat rt al., 1993). These hypotheses have
received support from recent physiological studies that correlated muscular con-
traction patterns with the kinematics of tunas during swimming (Knower et al.,
1999; Shadwick et al., 1999).
A detailed understanding of the mechanisms of swimming in tunas requires
additional study of the functional morphology of axial muscle, connective tissue,
and skeletal support. Previous research on the locomotor morphology of scombrid
fishes (Collette, 1978; Fierstine and Walters, 1968; Graham et al., 1983; Kafuku,
1950; Kishinouye, 1923; Nursall, 1956; Westneat et al., 1993) identified the key
components of the musculature, connective tissues, vertebral column, and caudal
skeleton that are involved in high-performance swimming of tunas. The position
of slow oxidative or “red” muscle has been a strong focus of this research due to
its role in tbermogenesis in tunas (Altringham and Block, 1997; Block, 1991;
Carey, 198 1; Graham, 1975; Rayner and Keenan, 1967). However, biomechanical
explanations of red muscle position and caudal fin musculoskeletal design have
not been proposed, and further research on myomere shape, connective tissue link-
ages, and vertebral mechanics will be necessary to develop a testable theory for
the mechanical design of tunas and mackerels.
This chapter contributes to a theory of scombrid locomotor mechanics by
summarizing recent work on morphology and modeling of scombrid fishes and
presenting new data on the functional morphology of myomeres, horizontal and
vertical septa, and the caudal fin. We review the literature on the structure of
muscle in scombrid fishes and use morphometrics of myomere shape to make
predictions about the generation and transmission of force during swimming.
Linked with the study of muscle are the key anatomical features of the horizontal
septum, including the robust system of tendons that connect myomeres to back-
bone and tail. To complement work on the horizontal septum, we describe the
connective tissues of the vertical septum and propose a mechanism of energy
storage and return involving the bending and twisting of neural spines. Also, we
present new information on the muscles, tendons, and bone of the caudal fin and
develop a biomechanical model of caudal fin function in scombrids. Finally, we
trace the distribution of some of the major locomotor features onto a phylogeny
of scombroid fishes to explore evolutionary patterns in the design for swimming.
II. EXTERNAL MORPHOLOGY:

BODY FORM AND FIN SHAPE
The degree of streamlining of body shape, cross-sectional profile, and design

of the caudal and pectoral fins are key features of the locomotor mechanism in
tunas (Collette, 1978; Fierstine and Walters, 1968; Magnuson, 1978). Body profile
and surface area are central to calculations of drag, and caudal fin shape is a key
determinant of thrust. Scombrids range from anteriorly thickened bodies with nar-
7. MECHANICAL DESIGN FOR SWIMMING 275
row caudal peduncles and highly lunate tails, such as tunas, to more streamlined
and slender bodies with relatively thicker peduncles and forked tails, such as the
Spanish mackerels. No detailed study of morphometrics on body shape or fin
shape has been performed for scombrids, although the methods of landmark mor-
phometrics and shape analysis (Bookstein, 1991) would apply nicely to functional
questions of body profile and fin shape.
Fortunately, several authors have published data on aspects of external mor-
phology that are functionally relevant. Magnuson ( 1978) published a table of line-
ness ratios (length/thickness) that are used as a metric of streamlining. Fineness
ratios ranged from about 4.5 in Thunnus and Euthynnus to 4.8 in Auxis, 5.6 in
Sarda, 6.2 in Scomber, and 8.4 in Acanthocybium. Magnuson and Weininger
( 1978) estimated external shape and surface area by tracing photographs of seven
species of tuna and applying a geometric model based on length, width, depth,
and a positional estimate for maximum depth. Their results showed that body
surface area was roughly proportional to the square of length, but that fin areas
were proportional to the cube of length. A preliminary comparison suggested that
for fish of the same length, the surface area of a mackerel was significantly lower
than that of a bonito and a bigeye tuna, suggesting that direct measurements of
surface areas and body profiles will be a critical data set for future hydrodynamic
modeling. A phylogenetic perspective (Figure 1) reveals that most basal scom-
broid groups (Gempylids, Trichiurids, and the billfishes) tend to have elongate
bodies, as do the mackerels (e.g., Scomber, Scomberomorus), and there is a trend
toward anterior thickening of the body and narrowing of the caudal peduncle in
the bonitos (Sarda) and tunas (Euthynnus, Thunnus).
Morphometrics of the caudal fin of scombrids have focused on aspect ratio,
an estimate of the degree to which a fin is winglike. Aspect ratio (AR) is calculated
as the fin span squared, divided by area. Aspect ratios were calculated by Fierstine
and Walters (1968) and Nursall ( 1956) and Magnuson ( 1978) summarized avail-
able data. The aspect ratios of scombrids range from about 4 to 9, with the closely
related billfishes such as the marlin (Mkzira) reaching an AR of 10 or above
(Figure 2). In general the mackerels (Scomber; Scomberomorus) have AR values
at the lower end of the scale. although the wahoo (Acanthocybium) is part of the
mackerel tribe Scomberomorini but has a higher AR of about 6. The bonitos (Sar-
dini) such as Sarda tend to have intermediate ARs, and the tunas (Auxis, Euthyn-
nus, and Thunnus) have slender caudal fins with relatively high spans, giving them
ARs between 6 and 9. Some diversity is apparently present within each scombrid
lineage, as Magnuson (I 978) lists the AR of the bluefin tuna, Thunnus thynnuu, as
low, around 5.5. Phylogenetic comparison (Figure I) indicates that high-AR tails
have evolved at least three times in the scombroids-in the billfishes, the wahoo.
and the tunas.
A complete survey of caudal fin shape variation in scombrids would contrib-
7.9-10. I AK=lO.O
Fig. 2. Caudal fin shapes and aspect ratios (AR) ranging from low in the mackerels to high in the
tunas and in the blue marlin. Caudal tin drawings adapted from Collette and Nauen (1983).
ute significantly to our knowledge of locomotor morphology. In addition to aspect

ratio, there is clear variation in the angle of dorsal and ventral caudal fin lobes,
and in the distribution of area of the fin. We discuss below the mechanisms of
caudal fin musculature, which allow dynamic changes in fin shape during the tail
stroke. As additional kinematic studies and swimming performance tests are done
with living tunas, analyses of the hydrodynamics around the flapping caudal fin
foil will reveal mechanisms of thrust uroduction.
III. AXIAL MUSCLE:

MYOMERES AND MYOSEPTA
Research on locomotor morphology in fishes has provided a basis for gencr-

ating and testing hypotheses of mechanical design for swimming (Alexander.
1969; Dickson, 1996; Mos and Van der Stelt, 1982; Nursall, 1956; Wainwright.
1983; Westneat et al., 1993; Willemse, 1959). A central goal of these studies has
been to develop mechanical hypotheses for muscle function. Alexander ( 1969)
considered the function of muscle segments (myomeres) by calculating muscle
fiber trajectories from the myoseptum to the vertebral column. Modeling of the
shortening of the fiber trajectories enabled calculation of the relative efficiency
and power output of several different muscle fiber arrangements. The model of
Mos and Van der Stelt (1982) predicted “infinitesimal” undulation movements
through consideration of a horizontal strip of muscle, but this model excluded
consideration of myomere geometry and the horizontal septum. Nursall (1956)
insightfully treated the myomeres as providing the force for a lever system that
bends the body due to serially arranged “flexures” of the myomeres. Although
Nursall’s model of bending did not consider the mechanism of force transfer
through the complex morphology of myomeres and septa, the model included a
means of calculating the mechanical advantage of the lateral tendons in the tail ot
a tuna. Wainwright (1983) considered the roles of many of the components
(muscle, tendon, skin, and skeleton) likely to contribute to the mechanism of force
transfer from muscle through tendon and skin to vertebrae and caudal fin. This
work highlighted the need to include in the model the tendons and other tissues
that contain collagen fibers and transmit forces. Finally, several Russian authors
published work on the muscle tendon systems of the locomotor apparatus of
fishes, including the Scombridae (Koval and Butuzov, 1986; Vronskii and Niko-
laichuk, 1988).
Segmentally arranged myomeres with collagenous myosepta are present in all
fishes, but in most scombroid fishes these structures are hypertrophied masses of
muscle with stout connective tissues. These systems of oriented collagen fibers
play a critical role in force transmission during swimming (Long et al., 1996:
Wainwright et al., 1978; Westneat et al., 1993). Connective tissue morphology in
the axial locomotor system of scombroid fishes was described by Kishinouye
(1923), Kafuku (1950), Fierstine and Walters ( 19681, and Westneat et al. (1993).
Each of these studies identified connective tissues leading from the musculature
to the backbone, and related these tissues to locomotion. Kafuku (1950) referred
to a “sliding mechanism of two tendons” that attaches to the medial red muscle
of tunas, and Fierstine and Walters ( 1968) described the structure of the caudal
tendons, including the “great lateral tendon” of the tunas. Westneat et (11.( 1993)
demonstrated that the collagen fibers forming the myosepta and the connective
tissues of the horizontal septum. described below, are critical to the mechanism of
undulatory locomotion in scombrid fishes. This study showed that the connective
tissues of the main horizontal septum are the mechanical center for transduction
of muscle contraction into bending moments of the backbone. Below, we survey
the complex shapes of myomeres and myosepta of scombroid fishes in relation to
their connections to vertebrae and skin, and focus on the orientation of two sets of
collagen fibers, the anterior and posterior oblique tendons, that are integrated into
a single system for transmission of locomotor force.
The basic design of myomeres and tendinous septa in the locomotor system is
present in virtually all fishes (Nursall, 1956; Gemballa and Britz, 1998; Patterson
and Johnson, 1995). A myomere is a set of muscle fibers that attach anteriorly to
one myoseptum and posteriorly to the next myoseptum. Muscle fibers are gener-
ally oriented longitudinally, but their fiber angle with respect to the long axis of
the fish varies across species and within a myomere (Alexander, 1969). In scom-
brid fishes a portion of each myomere is composed of red, slow-twitch aerobic
muscle, and the rest of the myomere is fast-twitch anaerobic muscle (Hochachka
et al., 1978). Each myoseptum is a collagenous sheet separating two myomeres
(Figures 3 and 4) that attaches to the backbone, vertical septum, and skin. The
myoseptum of scombrid fishes is formed of four major connective tissue cones.
Two of these point forward: one dorsal and one ventral to the horizontal septum.
These are the anterior-pointing cones (APCs; Figures 3 and 4). The myoseptum
has two large posterior-pointing cones (PPCs): one dorsal and one ventral to the
APCs. The dorsalmost and ventralmost elements of the PPCs extend forward as
the anterior-pointing arms (APAs; Figures 3 and 4).
Each myoseptum is a fabric of two tracts of collagen fibers, each tract having
different orientations (Figures 3 and 4). One tract of myoseptal fibers is oriented
generally longitudinally. A fiber starting near the tip of the anterior-pointing cone
will either merge with the skin or converge medially between the APCs to form
the posterior oblique tendon (POT: Figures 3-6). All POTS lie within the main
horizontal septum. In the other tract of myoseptal collagen fibers, the fibers loop
around the long axis of the APC at its base, where it meets the other APC. These
fibers continue medially where they attach to vertebral centra as anterior oblique
tendons (AOTs; Figures 3 -6), forming a second component of the main horizon-
tal septum. AOTs loop over the posterior half of the APCs and the anterior half of
the PPCs and attach to the vertical septum as secondary horizontal septa. Both the
longitudinal and circumferential tracts of fibers attach to the skin along the line of
the skin’s intersection with the APCs.
The cones and the connective tissues of the myoseptum that are visible in
Fig. 3. Lateral dissections of the left side of (A) Euthynnus alletteratus, (B) Scomberomorus
maculatus, and (C) Mukuira nigricuns, showing the shape of a myomere in the midbody region. An-
terior is to the left. APC, anterior-pointing cone; PPC, posterior-pointing cone; APA, anterior-pointing
arm: MHS, main horizontal septum; SHS, secondary horizontal septum.
AOT SHS
Fig. 4. Drawing of a myomere of Scomberomorus cuvalla in oblique view showing anterior-

pointing cones (APC), posterior-pointing cones (PPC), anterior-pointing arms (APA), anterior oblique
tendon (AOT), posterior oblique tendon (POT), and secondary horizontal septa (SHS). The main hori-
zontal septum (MHS) is formed between the APCs, where the AOTs and POTS converge.
lateral view vary among scombrid species. The APCs of Scomber (Westneat et al.,
1993) and Scomberomorus (Figure 3B) are shorter than those of tunas such as
Euthynnus (Figure 3A). The APCs of the blue marlin (Makuiru nigricuns) are
extremely long and show highly developed collagen sheets that converge to form
strong POTS (Figure 3C). In cross-section, it is seen that slightly fewer cones are
nested within a single transverse section of a mackerel than a tuna (Figure 5).
Differences in myomere shape are associated with variation in the number of ver-
tebrae spanned by the connections of AOTs and POTS to the vertebral centra.
Westneat et al. (1993) found that the AOT-POT “loop” of mackerels spanned
three to five vertebrae, whereas the loop of bonitos and tunas spanned five to seven
vertebrae. Thus, phylogenetic trends in this system are a dual origin of elongated
anterior-pointing cones, in both tunas and billfishes, and a trend toward a greater
number of vertebrae spanned by the AOT-POT system in the tunas (Figure 1).
Current quantitative models for the function of fish myomeres in exerting force
through tendons (Westneat et al., 1993) and through generation of intramuscular
pressure (Westneat et al., 1998) make predictions that depend on the dimensions
of the muscle cones, the arrangement of fiber angles in the muscle (Alexander,
1969), the geometry of the main horizontal septum (see below), and the positions
of red muscle regions in the myomere.
IV. AXIAL MUSCLE:

RED MUSCLE MORPHOLOGY
The position of red muscle is critical to the mechanism of undulatory loco-

motion, due to its connections to the POTS in both mackerels and tunas. Descrip-
Fig. 5. Transverse sections of the boJy r,t a mackerel and a tuna (A and B, S~,o/,ihr,ztmr,nr.\
wl~~/ln, 770 mm (standard length): C and D, Eurhwu~r dlrrtcrcrrus. 630 mm SL). Drawings he-
low each photograph illustrate important l~xomotor structures. Note the convergence of myosepta
of anterior-pointing cones to form the main horizontal septum. APA. anterior-pointing arms; APC’,
anterior-pointing cones; BB, hackbone; MHS. main horizontal \cptum: MYOS. myosepta: PPC‘.
po\rerior-pointin: cone\: SHS. sxxrndw~ hd,rl/~Wal wpt:~.
tions of red muscle distribution in scombrids (Fierstine and Walters, 1968; Gra-
ham et al., 1983; Kafuku, 1950; Kishinouye, 1923) have shown that mackerels
such as Scomber and Scomberomorus have laterally placed red muscle tissue, but
that tunas have their red muscle located internally, along the horizontal septum.
This difference in red muscle position is illustrated in lateral dissection (Figure 3)
in which the red muscle of the tuna is seen located along the medial slopes of the
anterior-pointing cones (Figure 3A) and the lateral red muscle cone of the mack-
erel is visible close to the skin attachment point (Figure 3B). Transverse sections
(Figure 5) also show that the mackerel red muscle is placed at the lateral tip of the
horizontal septum, and tuna red muscle lies internally along the horizontal sep-
tum. Interestingly, Surdu shows an intermediate state, in which red muscle is par-
tially internalized, so that a clear phylogenetic trend toward internalization of slow
oxidative muscle is seen from mackerels to bonitos to tunas (Figure 1).
The red muscle of the myomere of tunas plays a dual role: production of lo-
comotor forces and production of heat for endothermy (Graham, 1975; Carey,
198 1). Placement of red muscle volume affects the mechanics of locomotor force
transmission, When red muscle is placed laterally, as in the mackerels, it is well
positioned to exert forces directly to the POTS for transmission to the backbone.
Internal red muscle in tunas is always centered around the horizontal septum, and
often has a significant volume located laterally. Thus, it is positioned to pull di-
rectly on the long tendons (AOTs and POTS) of the horizontal septum. The me-
chanical advantage of internal red muscle is less than that of lateral muscle due to
its proximity to the backbone and due to the change in angle of insertion on the
POTS. However, Altringham and Block (1997) showed that the internally placed
red muscle generates significantly more power due to its warmth, suggesting a
possible trade-off between force from mechanical advantage and force from con-
tractile properties. Also, it is possible that internal red muscle in the posterior half
of a tuna may partially bypass the POT system and exert force directly on the
great lateral tendon that crosses the caudal peduncle and inserts on the hypural
plate. Shadwick et al. (1999) suggested that there may be shear between red and
white muscle components of the myomere due to the transmission of contraction
forces posteriorly to the caudal fin. A comparative approach to red muscle design,
twitch properties, and motor patterns is required to address questions of red
muscle function in its various configurations.
V. AXIAL CONNECTIVE TISSUES:

MAIN HORIZONTAL SEPTUM
The horizontal septum of scombroid fishes is a spectacular fabric of stout ten-

dons that is unparalleled among fishes. The main horizontal septum (MHS; Fig-
ures 3 and 5) is a layer of connective tissue that attaches to the backbone along the
midline, and extends laterally toward the skin between the anterior-pointing
cones. The horizontal septum is formed by the convergence of myosepta from the
APCs. The sheet of myosepta dives medially and attaches to the backbone (Fig-
ures 6 and 7). The MHS is the most conspicuous connective tissue structure, and
is composed of sturdy white bands of parallel collagen fibers (Figures 6 and 7).
These collagen fibers of the MHS come from two prominent connective tissue
structures that have different orientations: the anterior oblique tendons (Figures 4.
6, and 7) and the posterior oblique tendons (Figures 4, 6, and 7). This crossed-
fiber array of AOTs and POTS was first described by Kishinouye (1923) in tunas
and then by Kafuku (1950) in mackerels. A comparative and mechanical analysis
of this tendon system was presented in Westneat et al. (1993).
The anterior oblique tendons (Figures 4, 6, and 7) are circumferential bands
of collagen fibers within the myosepta that surround the bases of the APC and
PPC. The AOT fibers attach to the vertical septum and the neural and hemal
spines, contributing to the secondary horizontal septa. Medial AOT fibers form
discrete tendons that angle anteriorly as they dive to the backbone. The anterior
oblique tendons are specialized, hypertrophied versions of epipleural and epicen-
tral tendons that are present in a broad diversity of teleostean fishes. Patterson and
Johnson (1995) surveyed these tendons and their ossifications as intermuscular
bones in teleosts (incorrectly referring to the connective tissues as ligaments), and
Gemballa and Britz (1998) added information to that survey by the use of polar-
ized light. The AOTs in the horizontal septum are often closely associated with
epipleural ribs. Epipleural ribs, when present in a particular segment, articulate
with the vertebral centrum and extend laterally within the main horizontal septum
(Figure 6). Every epipleural rib has AOT collagen fibers running along its edges.
When the bone of an epipleural rib ends laterally, AOT fibers continue from its
tip to contribute to the myoseptum. Epipleural ribs are likely to be ossified serial
homologues of the AOTs that occur in the main horizontal septum, and increase
tensile strength of the AOT.
The AOTs are variable among scombrid fishes in their number, structure, and
angle of orientation to the backbone (Westneat et al., 1993). There is a phyloge-
netic trend toward more cordlike and robust AOTs that insert at a more perpen-
dicular angle to the backbone as one moves up the phylogeny from mackerels to
bonitos to tunas (Figure 1). In Scomber and Scomberomorus, an AOT is a band of
collagen fibers attaching to the posterior edge of the epipleural ribs in the anterior
region of the body. The first AOTs without ribs, located in the anterior half of the
caudal region, attach along the lengths of the vertebral centra. The anterior AOTs
insert at about a 45”-55” angle to the backbone in Scomber, Scomberomorus, and
Acunthocybium, but this angle gradually increases posteriorly, until each AOT is
a continuous sheet of fibers at 75”-80” to the backbone (Figure 7).
The AOTs of the wahoo (Acarathocybium) are narrow on the first 9-l I ver-
tebrae where they attach to the posterior edge of epipleural ribs (Figure 7). On
vertebrae 32-48, the AOTs are wider and insert on ‘Y2to 3/4of the centrum length.
At vertebrae 49-54, the AOTs become narrow again, correlated with broad inser-
tions of POTS. The AOTs of Surdu, Euthynnus, and Thunnus (Figure 6) differ from
those of the mackerels and wahoo in several ways. Most AOTs in these taxa sur-
round epipleural ribs. Epipleurai ribs and associated AOTs are present on the first
32 vertebrae, but are absent on the bony keel, a series of tightly connected vertebrae
in the peduncle region (Collette and Chao, 1975). Bands of AOT fibers occur on
both the posterior and the anterior edge of each epipleural rib. At the tip of each epi-
pleural rib in both mackerels and tunas, a band of stout collagen fibers splays out to
form a thick lateral portion of the AOT. This collagen band passes around a POT,
forming a “sling” through which the POT passes. After forming the sling, the AOT
splits into two groups of fibers. One group extends dorsally and one ventrally as
they form the circumferential bands around the APCs. The angles of the AOTs of
Surda, Euthynnus, and Thunnus range from about 50” to the backbone anteriorly to
about 80”-90” near the tail (Westneat et al., 1993).
The posterior oblique tendons (Figures 4,6, and 7) are a second set of robust
bands of collagen in the main horizontal septum. These tendons are formed from
the longitudinal collagen fibers of the myosepta of anterior-pointing cones as these
fibers converge posteriorly and laterally. In the mackerels, the POTS start where
the longitudinal fibers of the two APCs meet midlaterally, just medial to the red
muscle, to form a discrete tendon. POTS angle posteromedially, within the MHS,
to attach to the lateral edge of the vertebral centra. As a POT extends posterome-
dially toward the backbone from its lateral origin, it passes through the series of
AOT slings, forming a crossed fiber array with the AOTs (Figures 6 and 7).
Scombrid species vary in the structural details of the POT and in the insertion
points of the POTS along the backbone (Westneat et al., 1993). There is a phylo-
genetic trend toward more robust POTS that insert at a lower angle to the backbone
as one moves up the phylogeny from mackerels to bonitos to tunas (Figure 1). In
Scomber and Scomberomorus the anterior-most POT is a thin band of collagen
fibers. The angle relative to the backbone of the anterior POTS is around 45”
in Scomber, and 60”-75” in Scomberomorus. POTS that attach to the posterior
vertebrae are strong tendons that attach to the posterior % of the centrum (Fig-
ures 6 and 7). POT angles are acute in this region in the mackerels, ranging from
__- -__
Fig. 6. Morphology of the main horizontal septum (MHS) in Thnnus obesus (845 mm SL) in
the region of (A) vertebra 20, (B) vertebra 25, and (C) vertebra 30. View is of the right side, dorsal
surface of the MHS (neural spines point toward the reader at the bottom of each picture). Anterior is
to the left. The MHS extends laterally to the point where AOTs and POTS meet, and the reflected
myomeres are seen above the MHS in each image. The anterior oblique tendons (AOT) run from the
vertebrae (V) up through the red muscle to the skin, becoming more perpendicular to the vertebral
column posteriorly. AOTs in the anterior region surround epipleural ribs (EPR). The posterior oblique
tendons (POT) have a shallower angle of insertion on the vertebrae posteriorly.
a minimum of 12” in Scomberomorus to around 20” in Scomber. The wahoo

(Acanthocybium) POTS are similar in angle and position to those of the mackerels.
although POTS in the wahoo often insert on more than one vertebral centrum, and
posterior POTS are wide at the vertebral insertion, sending some fibers to the ccn-
tra anterior and posterior of the main attachment point.
The POTS of Surdcl, Euthynnus, and Thunnus are different in several ways
from those of the mackerels. Tuna POTS have a low angle to the backbone, rang-
ing from about 40” anteriorly down to 1O”-15” posteriorly. Tuna POTS are long,
spanning five or six AOTs. All POTS in the tunas have branching of the main
bands of collagen fibers into smaller tendons (Figure 6). The anterior POTS insert
on the centrum and on the ventral surface of an epipleural rib. The POTS that
attach mainly to vertebrae IS-25 have up to four branches (Figure 6A). The effect
of POT branching in tunas is that each segment of the axial skeleton is inserted
upon by the connective tissues of multiple myomeres and each myomere pulls on
multiple centra. Horizontal septum geometry and the lengths and angles of inser-
tion of the AOTs and POTS are central components of biomechanical models of
locomotor function in the Scombridae.
VI. MUSCLE FUNCTION: TENDON LINKAGES

IN THE HORIZONTAL SEPTUM
Hypotheses regarding locomotor mechanics in fishes must include an expla-

nation of the transfer of muscle force through the complex connective tissues of
the myosepta and horizontal septum. Myosepta and horizontal septa are the tissues
that transfer forces from the contraction of myomeres to the backbone and caudal
fin during locomotion in scombrids (Fierstine and Walters, 1968: Wainwright,
1983; Westneat et al., 1993). The geometry of the myomeres, the position of red
muscle, and particularly the geometric conformation of crossed-fiber arrays of
collagen in the main horizontal septum suggest three complementary mechanisms
that contribute to body bending in scombrid fishes: (1) direct pull upon the array
of posterior oblique tendons in the horizontal septum by myomeres, (2) increase
in the tension of the connective tissue system by hydrostatic pressure created by
Fig. 7. Morphology of the main horizontal septum (MHS) in Acunrhoc,yhium solmdri (I 120 mm
SL) in the region of (A) vertebra 20. (B) vertebra 0, and (C) vertebra 40. View is of the right side.
dorsal surface of the MHS [neural spines (NS) point toward the reader at the bottom of each picture).
Myomeres (MYO) are reflected above the MHS. Anterior is to the left. The anterior oblique tendons
(AOT) run from the vertebrae (V) up through the red muscle (RM) to the skin, becoming more per-
pendicular to the vertebral column posteriorly. Both AOTs and POTS are Ratter and broader in the
wahoo than in the tuna.
the swelling of contracting muscles, and (3) muscles that exert force directly onto
the caudal fin. Quantitative models of these mechanisms permit calculations of
mechanical advantage of muscle and can account for locomotor specializations
occurring in scombrid fishes.
The mechanism of force transfer through the MHS via the POTS may be mod-
eled as a lever system for exerting forces on the backbone to cause bending (West-
neat et al., 1993). The amount of force from contracting muscle that is applied to
the backbone in a bending moment is determined by the length of the POT, the
angle of the POT to the backbone, and the lateral distance from the backbone of
the AOT-POT sling. A quantitative model of the main horizontal septum (Fig-
ure 8) makes it possible to predict the action of a muscle segment in terms of the
amount of force or displacement moment applied to the vertebrae by the AOTs
and POTS.
The mechanics of mackerel and tuna myomeres can be compared by using the
velocity ratio (the reciprocal of the mechanical advantage) as a measure of the
transmission of motion through the POTS (Westneat et al., 1993). The velocity
ratio is the ratio of output motion to input motion of the system, and lateral dis-
placement is the sine of the AOT-backbone angle times the length of the back-
bone segment. The geometry of the system at rest is two-dimensional (Figure 8A),
allowing calculation of the angles and distances involved in the force transmission
system.
Shortening of red muscle pulls on the POT and draws it through the AOT
slings (Figure SB). The model calculates the total angular rotation of the backbone
at the joint between vertebrae posterior to the insertion of an AOT (Figure 8B). If
the total angular rotation over all joints is divided evenly over the three interver-
tebral joints spanned by the AOT and POT, the model can predict total angular
rotation due to a single unit of muscle. Westneat et al. (1993) simulated 10%
muscle contractions in a mackerel (Scomberomorus cavalla) and a tuna (Euthyn-
nus alletterutus). For the mackerel, a muscle contraction of 5.5 mm caused a total
angle change of about 10” distributed over three intervertebral joints, or an angle
of about 3.3” at each intervertebral joint to produce the bent backbone. The lateral
displacement of the backbone at the point of attachment of the POT was calculated
to be 11.3 mm. The velocity ratio of the system is the ratio of output motion
(11.3 mm) to input motion (5.5 mm), which equals 2.05.
In the Euthynnus horizontal septum, the POT is longer and has a lower angle
to the vertebrae, and the effective bending force of the tendons spans more inter-
vertebral joints (5-7) than does the mackerel (3). A 10% muscle shortening pro-
duces a total angle change among intervertebral joints of 18.2”. Distributed over
five intervertebral joints, this results in a rotation at each joint of 3.6”. Displace-
ment at the posterior end of the tuna POT is 25.8 mm, over twice the displacement
result of the mackerel. The velocity ratio is also larger: 25.8 mm/7.5 mm = 3.4.
Thus, the tuna has a displacement advantage that is one-third greater than the
7. MECHANICAL DESIGN FOR SWI’MMING
POT
red muscle
contraction
3 bending
Fig. 8. Mechanical diagrams of the biomechanical model of the AOT-POT mechanism for ver-
tebral bending in scomhrid fishes. Anterior is to the left. (A) Geometric position of the mechanism of
Scomberomorus cavallu at rest. t B) Contraction of red muscle through the AOT slings causes the
backbone to bend. (C) The geometry of the MHS mechanism of Euthynnus ulletrerutus at rest. Mor-
phometrics and angle calculations can be u\ed in the model to calculate bending at each intervertebral
joint.
mackerel. The mechanical (force) advantages of the two designs are the inverse of
the velocity advantage (about 0.5 for the mackerel and 0.3 for the tuna).
Research on the mechanical properties of bending in backbones has shown
that the angular stiffness of the backbone around the intervertebral joints deter-
mines the amount of mechanical work (force times distance) that muscle must do
over a complete cycle of bending (Long, 1992). Because the backbones of scom-
brids. and particularly tunas, have many features that contribute to their flexural
stiffness, we suggest that undulation of the backbone in scombrids requires high

force advantage rather than velocity advantage. The higher angle of the mackerel
POT to the backbone is better suited to a forceful lateral pull than that of tunas.
The long, low angled POT of tunas is perhaps better suited for energy storage in
elastic recoil, because elastic recoil length is proportional to length of the tendon
(Alexander, 1988). The angle of the POTS is variable from head to tail in scombrid
fishes, starting high anteriorly and ending low posteriorly. This geometry suggests
design for force advantage anteriorly, smoothly transforming to a displacement
advantage posteriorly. Future research on this force transmission system might
focus on quantitative analysis of the AOT-POT system in a broader range of
scombrid fishes and other taxa. Equipped with biomechanical models, such re-
search could predict the functional role of variation in connective tissue design,
and the model could be tested with direct measurement of body bending and
forces in the tendons of the posterior region of the fish.
VII. MUSCLE FUNCTION: PRINCIPLES

OF HYDROSTATIC PRESSURE
In current models of myomere function and the mechanics of the horizontal

septum (Figure 8), an important mechanism is that of maintaining the lateral po-
sition of the POT. This is the moment arm of force application to the backbone.
The sling mechanism of the AOTs (Figure 8) functions as a tensile standoff that
maximizes the mechanical advantage of the POT’s lateral pull. By holding the
AOT-POT junction away from the backbone, the sling prevents mediad displace-
ment of the cradled POT during bending. This system is analogous to a “jib”
mechanism used in mechanical engineering. A jib is an extra strut, usually with a
pulley on the end, that is added perpendicular to the direction of force to increase
the length of the effort arm of a lever (Vogel, 1988). The role of the AOT sling is
thus to increase the moment arm of the force from the muscle applied to the back-
bone. In order for the AOT to hold the POT away from the backbone like a jib it
is necessary to put the AOT into tension. The mechanism of production of tensile
forces in the AOT involves hydrostatic pressure.
Hydrostatic pressure is generated for the purpose of putting connective tissues
in tension by a mechanism involving the anterior-pointing cones of white muscle
(Figures 3 and 4). The term “muscular hydrostat” (Kier and Smith, 1985) refers
to muscular systems of constant volume that can exert lateral pressure forces when
they contract. Kier and Smith (1985) demonstrated that decrease in length of a
constant volume cylinder inevitably results in an increase in radius, and vice versa.
This fact is used by organisms in numerous mechanisms for force transmission
without rigid skeletal elements (Smith and Kier, 1989).
The same principle can be applied to the structure of myomeric cones, substi-
7. MECHANICAL DESIGN FOR SWIMMING
V = nr2h
3
Fig. 9. (A) Mechanical diagram of the mechanism of generation of intramuscular pressure. Pres-
sure changes by contraction and radial expansion of muscle cones. A cone of length (height) h and
radius r, shortens, causing a local increase in radius to rz. The radial swelling of the cones (shown in
cross-section) causes an increase in hydrostatic pressure (P) in the space bounded by backbone, septa.
and skin because these structures resist the expansion. (B) The relation between length and diameter
for a cone of constant volume. Curves for actual cone volumes of Sconrheromorus cavulla and EN-
thynnus nlletrerarus are shown. with the resting dimensions of real myomeric cones indicated.
tuting the equation for the volume of a cone for that of a cylinder (Figure 9A).
When a cone of muscle contracts, the fact that the volume remains constant causes
the cone to swell, increasing the radius of the cone’s base (Figure 9). Westneat
et al. (1993) used morphometric data on cone geometry to model the contraction
of the anterior-pointing cone of Scomheromorus cavu/l~ and Euthynnus allette-
rutus. Their calculations showed that a 10% muscle shortening for both species
resulted in a 5% increase in radius.
Muscular hydrostats will stiffen as they contract if they are wrapped with high-
tension fibers that resist radial expansion (Kier and Smith, 1985; Wainwright
rt al., 1976). The mechanics of fiber-wound, pressurized cylinders depend upon
the relations between length, diameter, skin stress, and wall thickness (Quillen,
1998). For a cylinder, circumferential stress due to internal pressure is twice lon-
gitudinal skin stress (Wainwright et ul., 1976). For a cone, the relationship be-
tween internal muscle pressure expanding laterally depends on total longitudinal
muscle force, cone shape, and cone volume. This is so because when the constant-
volume longitudinal muscle cone contracts, it expands radially and increases the
stress of the circumferential collagen fibers (Figure 9; Westneat et al., 1993).
Internal muscle pressure is proportional to the degree of radial expansion of
the cone.
A quantitative model of intramuscular pressure generation in fish muscle was
developed by Westneat et al. (1998) for two nonteleostean actinopterygian fishes,
Polyptet-us and Amia. Here we apply that model to mackerel and tuna muscle, in
which the muscle cone of Scomheromorus muculutus has a volume of 19.5 cm3
(h = 9.5 cm, r = 1.4 cm) and the cone of E. alletterutus a volume of 106.2 cm3
(h = 15.0 cm, r = 2.6 cm). The model starts with the relationship between the
length (h) and radius (r) of a cone-shaped, constant-volume muscular hydrostat
(Figure 9). The volume of a cone is
s-r2h
V=--- (1)
3
For a muscle cone of constant volume V, the relation between height and ra-
dius of the cone is
F
yz
J -3v
rh
This equation, when solved for a range of cone shapes with the volume of the
(2)
scombrid cones (Figure 9B), reveals that changes in cone length, due to muscle
contraction, translate into substantial radial expansion over a limited range of cone
geometries. The resting geometries of the mackerel and tuna muscle cones are
both positioned in the region of the curve where muscle shortening begins to be
transmitted into increasing radial force, but before the exponentially increasing
slope of radial expansion (Figure 9s). Thus, changes in intramuscular pressure
occur without large changes in cone dimensions.
To calculate longitudinal muscle force, we used the equation of Calow and
Alexander ( 1973) for a muscle whose fibers are at an angle to the primary direc-
tion of force,
F, = $ 6sin2a (3)
where V = volume, d = diameter, 6 = muscle fiber force, and LY= muscle fiber
angle to the long axis of the muscle. We used Altringham and Johnston’s (1982)
estimate of muscle fiber force per unit area in fish white muscle: 200 kN/m2, and
Alexander’s (1969) measurements of muscle fiber angles in the myomeres of
Scomber scombrus (30”). Longitudinal muscle forces calculated using this equa-
tion for the cones of S. maculatus and E. ulletteratus were 1.2 and 3.5 N (new-
tons), respectively. Muscle force and fiber angle will likely vary among species
and affect the force of muscle contraction.
In a cone-shaped muscular hydrostat, changes in longitudinal force are trans-
mitted to radial force by the relationship between cone length and cone diameter
(Figure 9B). Kier and Smith (1985) suggested that this mechanism in cylindrical
muscular hydrostats is similar to that of a lever system, where the dimensions of
the hydrostat determine lever mechanics. For a lever, the output force transmission
(F,) equals the product of input force (Fi) and in-lever length (Li) divided by out-
lever length (L,,). We propose that the transmission of force from longitudinal to
radial is proportional to the change in cone dimensions during a muscle contrac-
tion. We calculated radial force by the equation
Ah
(4)
Fs = Fi . G
Radial muscle forces for the average cones of S. maculatus and E. alletteratus
were 7.6 and 18.8 N. These data illustrate that longitudinal shortening forces can
be magnified by the properties of a fiber-wound, constant-volume, hydrostatic
muscle, similar to the properties of fiber-wound cylinders (Wainwright et ul.,
1976). The force transmission advantage (Ah/Ad) of S. maculatus was 6.2,
whereas that of E. alletterutus was 5.3.
To compute pressure in kilopascals (kilonewtons per square meter), we di-
vided radial force by the surface area of the curved portion of the cone:
SA = TTT-I,where 1 = v’+ (5)
Pressures calculated using the model for the average cones of S. muculatus and
E. alletteratus were 156 and 130 kPa (slightly over 1 atm of pressure). These
estimates depend upon little or no collagen fiber extension, in which the Young’s
modulus (E = stress/strain) is high. These predicted values are in the range of
intramuscular pressures measured in sharks (Wainwright et ul., 1978) and in basal
actinopterygian fishes (Westneat et al., 1998).
The functional role of intramuscular pressure is to expand radially and in-
crease the stress of the circumferential AOT fibers (Figures 3-6). Modeling re-
sults are consistent with the hypothesis that the AOT must be put into tension to
act as a jib for the action of the POT, thus maximizing the amount of lateral force
applied to the backbone. The amount of tension required in the AOT during lo-
comotion is likely to be affected by the degree of support given by epipleural ribs,
and by the relative force or velocity advantage of the POT (i.e., POT angle). If,
however, only red muscle fibers contract during locomotion, then the mechanism
of the anterior-pointing cones will function somewhat differently. In mackerels.
most red muscle lies laterad of the APC, in a separate region along the lateral
midline (Figure 5). Contraction of this muscle would contribute little to increased
pressure in the APC. The red muscle of tunas, on the other hand, is located medi-
ally within the boundary of the APC myosepta (Figure 5). Contraction of tuna red
muscle will cause increased pressure within the APCs and increased tensile forces
in the AOT. This may contribute to the higher apparent stiffness of the anterior
portion of the tuna’s body during locomotion.
An additional physical principle influences the way in which oriented collagen
fibers of AOTs and those within the skin can be put into useful tension by hydro-
static pressure created by contracting muscle. The skin of a pressurized, constant
volume cylinder reinforced by a crossed helical fiber array and inflated circumfer-
entially will decrease in length with a force that is the circumferential force mul-
tiplied by the tangent of the fiber winding angle (Wainwright et al., 1978). The
crossed helical collagen fiber array in the skin of scombrids, with angles of 55” to
the long axis and higher, ensures that longitudinal strains will be larger than cir-
cumferential strains. Because this fiber arrangement constrains extension of the
radius of the main APCs and of the muscle mass in general, the swelling of the
contracting muscle is responsible for putting the entire connective tissue array,
including horizontal septa and skin, into tension.
Phylogenetic analysis of the mechanisms by which fish muscular hydrostats
function must await further testing of the model and survey of cone shapes among
taxa. Further study of muscle pressure variation and myomere morphology will
reveal the effects of cone geometry on intramuscular pressure mechanisms across
taxa and help to refine mechanical models of pressurized vertebrate musculoskele-
tal systems. To test hypotheses of this model, subdermal pressure measurements
similar to those recorded for sharks (Wainwright et al., 1978) and for basal acti-
nopterygians (Westneat et al., 1998) should be recorded among scombrid species.
VIII. MECHANICAL DESIGN OF THE

CAUDAL FIN MUSCLES AND TENDONS
The functional morphology of fish caudal fins has been studied in a variety of
fish taxa (Bainbridge, 1963; Nursall, 1963; Videler, 1975; Lauder, 1989), but few
studies have considered the role of internal caudal structure for the mechanisms
of propulsion in scombrids (Fierstine and Walters, 1968; Gibb et al., 1999). In
scombrid fishes, large tendons from the myomeres attach in the caudal region, and
there is a set of muscles in the caudal peduncle and the fin that are separate from
the serial myomeres. There are thus two systems controlling caudal fin propul-
sion-myomeric tendons powered from body muscle, and the mechanical design
of intrinsic caudal muscles and their tendinous insertions on the fin.
In the caudal peduncle of both mackerels and tunas, the terminal five to six
myosepta lack POTS, AOTs, and circumferential fibers. Nevertheless, the conver-
gence of myosepta to form locomotor tendons is particularly striking in the caudal

region, where three robust collagenous structures are present: (1) the subdermal
sheath (SDS), (2) the great lateral tendon (GLT), and (3) the medial caudal tendon
(MCT; Figures 10-12). The subdermal sheath is a thick layer of collagen fibers
underlying the skin. The SDS is particularly thick in the area beneath the fleshy,
lateral keel. The SDS is formed from a fusion of cross-fibered collagen fibers at
the posterior end of the septa of the anterior-pointing arms, one epaxial and one
hypaxial. The SDS attaches to the hypural plate medially, and onto the caudal fin
rays ventrally and dorsally.
The great lateral tendon (Figures 10-12) is made of nested myosepta of ante-
rior-pointing cones, the bulk of which are derived from the last five to six myo-
septa. Longitudinal fibers are predominant in this tendon. Each cone that contrib-
utes to the GLT is a long tube of collagen attaching to the hypural plate of the
caudal fin (Figure 10). These collagen fibers in the GLT are likely homologous to
POTS that have shifted insertion to the caudal skeleton. The GLT attaches medi-
ally to the hypural plate, and has a broad aponeurosis onto the bases of the caudal
fin rays (Figures 11 and 12). A second set of caudal tendons is formed where the
collagen fibers of the posterior PPCs fuse, as a continuation of the SHS, to become
the medial caudal tendon (MCT), which underlies the GLT (Figure 10). The MCT
inserts on the hypural plate medial and anterior to insertion of the GLT.
Nomenclature of caudal muscles is now relatively stable, although previous
work on fish caudal fin musculature has used a variety of names for the same
muscles. Videler (1975) included a table of synonyms of caudal muscles, but used
names for muscles of Tilapiu that are not now in use. Other authors (Lauder, 1989:
Gibb et al., 1999) have followed Winterbottom’s (1974) synonymy, and that con-
vention is followed here. Scombrid fishes have a reduced number of intrinsic cau-
da1 fin muscles relative to other percomorph fishes, and other muscles have been
reduced in size. Gibb et aZ. (1999) described just two caudal muscles in Scomber
juponicus (the hypochordal longitudinalis and interradialis), but in dissections of
both Scomber scomber and S.japonicus, we found six nonmyomeric muscles that
attach to or are intrinsic to the caudal fin. Present in all mackerels and tunas we
have examined (Scomber, Scomberomorus, Acanthocybium, Sarda, Euthynnus,
and Thunnus) are the hypochordal longitudinalis. flexor dorsalis, flexor ventralis,
infracarinalis, supracarinalis, and interradialis (Figures 1 l-12).
The hypochordal longitudinalis (HL; Figures 11 and 12) is an unpaired struc-
ture on both sides of the caudal fin that originates on the hypurapophysis, a lateral
hooklike process of the parhypural (Figure 13) and inserts on the bases of the
sturdy central tin rays of the dorsal caudal fin lobe. In tunas, the muscle fibers are
greatly reduced or absent, leaving the structure as a hypochordal longitudinalis
ligament in Thunnus (HLL; Figure 11B). Note that the structure is not technically
a “tendinous remnant” as described by Fierstine and Walters (1968), because con-
nective tissues without muscle, extending from bone to bone, are ligaments. In
mackerels and other scombrids, the muscle fibers are more robust, and may be
Fig. 10. Modified posterior myomeres in Euthynnus alletteratus (550 mm SL) including (A) the
subdermal sheath (SDS) and the tendinous attachments from myomeres (MYO) to the caudal skeleton
and (B) the anterior-most myomere in which the POT contributes to the great lateral tendon (GLT)
that attaches to the hypural plate (HP). Note the elongated shape of the anterior-pointing cones.
(C) Modified posterior myomeres (MYO), great lateral tendon (GLT), and medial caudal tendon
(MCT) in Scomberomorus cavalla, 620 mm SL. Adapted from Westneat et al. (1993).
functionally implicated in asymmetry of the tin beat, in which the dorsal lobe of
the caudal fin leads the ventral lobe (Gibb et al., 1999).
The flexors ventralis and dorsalis together form a pair of muscles on each side
of the caudal tin that originate on the vertebral centra of preural vertebrae 2 and 3
(including the “keel” region in tunas) and insert via a tendon onto the posterior
Fig. 11. Caudal fin musculature of yellowfin tuna, Thunnus albacures, in (A) superficial dissec-
tion with skin removal, and (B) deep dissection after removal of great lateral tendon and aponeurosih.
AN, aponeurosis; CRF, modified causal ray flaps; FD, flexor dorsalis muscle; FT, flexor tendon; FV,
flevor ventralis muscle; GLT, great lateral tendon; HLL, hypochordal longitudinalis ligament; IR. in-
terradialis muscle. Scale bar = 5 cm.
7. MECHANICAL DESIGN FOR SWIMMING 2YY
hypural plate and onto the bases of the fan-shaped central caudal fin rays (here
named caudal ray flaps-Figures 1I-13). Their function in scombrids has not
been studied, but based on positional information, they are responsible for ab-
ducting (not flexing, despite their names) the caudal fin flaps from side to side to
increase or decrease the camber of the caudal fin during the propulsive stroke
(Figure 14).
The infracarinalis posterior and supracarinalis posterior originate on the poste-
rior-most pterygiophores supporting the last anal and dorsal finlets and insert on
the anterior-most caudal fin rays of the ventral and dorsal fin lobes. The functional
role of these muscles remains unexplored, but contraction of these muscles is
likely to “flare” the tail, protracting the dorsal and ventral caudal fin lobes.
thereby increasing the aspect ratio.
The interradialis is a muscle complex that invests the caudal fin rays in the pos-
terocentral region of the fin, attaching the caudal ray flaps to one another and to the
more fused dorsal and ventral lobes of the caudal fin (Figures 1 l- 13). Gibb et LE/.
(1999) discovered that the caudal fin of Scu&erjllponicus undergoes cycles of dor-
soventral expansion and contraction, with the tin maximally contracted at maximal
lateral excursion, and expanded as the fin crossesthe midline. The position and fiber
directions of the interradialis in mackerels and tunas support their suggestion that
the muscle is a retractor or depressor that decreases the dorsoventrai span of the tail.
The interradialis and posterior infra- and supracarinales muscles thus form an an-
tagonistic set of muscles for control of fin aspect ratio (Figure 14).
The evolution of the caudal muscles and their functional roles in body-caudal
fin locomotion in fishes was outlined by Lauder (1989). Lauder’s review and syn-
thesis identifies the lines of action of the caudal muscles in a diversity of fishes,
from basal taxa with heterocercal tails to teleosts with homocercal tails. Lauder’s
(1989) study highlights the need for functional studies of the intrinsic caudal
muscles, focusing on the role of the hypochordal longitudinalis in creating an
asymmetrical tail stroke by the homocercal tail. For scombrid fishes, a similar
approach is warranted, in which mechanical hypotheses for the caudal fin are
tested with kinematic data analysis of muscular motor patterns, and framed within
a phylogenetic hypothesis of scombrid relationships.
Hypotheses for the role of caudal muscles in scombrids are proposed based on
their origins and insertions on the caudal skeleton (Figures 13 and 14). The pri-
mary action of sweeping the high aspect-ratio tail is driven by the axial muscula-
ture and force transmission via the AOT-POT system and by the great lateral
Fig. 12. Caudal fin musculature of wahoo, Acunrhoc~~hirtrn dtrndri, in (A) \uperfictal dishcctron
with skin removal, and (B) deep dissection after removal of great lateral tendon and aponeurosis. AN.
aponeurosis; CRF, modified caudal ray flaps; FD, flexor dorsalia muscle: FT. flexor tendon; FV, tlevot
ventralis muscle; GLT, great lateral tendon: HL. hypochordal longitudinalis muscle; IC. infracarinale\
muscle; IR, interradialis muscle; MYO. myc)meric rnuccle. Scale har 5 in,.
Fig. 13. Morphology of the caudal fin skeleton in (A) Scomberomorus maculatus, (B) Acantho-
cyhium solundri, (C) Thunnus albacares, and (D) Tetrapturus angustirostris. Scombroid fishes are
variable in the morphology of neural and hemal spines, the caudal keel, and the modified caudal fin
ray flaps on the trailing edge of the fin. CK, caudal keel; CR, caudal rays; CRF, caudal ray flaps; HA,
hypurapophysik: HP, hypural plate: HS. hemal spineu: NS. neural spines.
FD
FV
Fig. 14. Mechanical diagram of the function of the cat&al fin musculature of scombroid fishes.
This is a generalized model for tunas, mackerels, and biilsshes (red = muscle; blue = tendon).
(A) The major force transmission pathway for tail thrust is from myomere (MYO) to great lateral
tendon (GLT), to tendinous aponeurosis (AN), to the hypural plate and leading edge of the caudal fin.
Also shown is the mechanism of interradialis (IR) control of the spread of the caudal ray flaps (CRF).
(B) The mechanisms of tail fin control by intrinsic caudal musculature. The dorsal and ventral flexors
(ED, FV) pull on the medial caudai tendons (MCT) to control the angle of attack of the caudal ray
flaps (CRF). The supracarinalis (SC) and infracarinalis (IC) insert tendinously on the leading edge and
protract (flare) the tail. The hypochordal longitudinalis (HL) controls the dorsal leading edge, likely
functioning to control tail stroke asymmetry.
tendons and medial caudal tendons (Figure 14A). The large forces transmitted
through the GLT are distributed broadly to the hypural plate by large tendinous
aponeuroses (AN; Figure 14A). We suggest that mackerels and tunas have consid-
erable control over fin shape through action of the caudal muscles. The fin span
and vertical profile of the fin can be dynamically altered during the caudal stroke
by the carinales muscles and interradialis antagonists (Figure 14). This mechani-
cal design likely provides a means for changing the aspect ratio of the caudal fin
with swimming speed or with tail position during the stroke, as observed in Scom-
ber (Gibb et al., 1999).
The central, posterior margin of the fin is formed by modified caudal fin rays
that are similar in shape and position to the “flaps” on the rear margin of aircraft
wings (Figures 11-14). In all scombroid fishes examined, the dorsal and ventral
flexor muscles can alter the angle of these caudal ray flaps. In an aircraft wing,
flaps are located on the aft or “trailing edge” of the wing and increase both lift
and drag (McCormick, 1974). Because of the increased drag, flaps are only par-
tially extended on takeoff, and fully extended on landing. Flaps extend downward
and rearward, thereby increasing both camber and wing area. The greater the
wing’s camber, or curvature, the better the wing will perform at slow air speeds,
due to the greater lift generated. Tunas and mackerels may adjust the camber and
the lift vectors of the caudal fin in a similar manner, during changes in forward
velocity or dynamically during the fin stroke as angles of attack change relative to
the water flow. Testing hypotheses of caudal fin muscle function will require data
on EMG profiles of locomotor muscles (Jayne and Lauder, 1995; Shadwick et al.,
1999) and force measurements on the large tendons that transmit locomotor forces
(Knower et al., 1993).
IX. THE BACKBONE AND VERTICAL SEPTUM
The mechanics of vertebral function in fishes have been analyzed from the
perspective of energy storage, dynamic oscillation, and the properties of stiffness
and damping that influence the transmission of waves of bending during swim-
ming (Hebrank et al., 1990; Hebrank, 1982; Long, 1992; Long and Nipper, 1996).
The vertebral column of scombrid fishes possesses enlarged neural and hemal
spines, and zygapophyses that articulate from one vertebra to the next, suggesting
that scombrid backbones may have a relatively high stiffness (Figure 15). Tunas
have bony processes extending between hemal spines that may also increase stiff-
ness (Figure 15B), and the hypural plates are completely fused in tunas, providing
a solid attachment point for robust tendons. Hebrank (1982) found that skipjack
(Kutsuwonus) backbones had high stiffness relative to nonscombrids, and other
Fig. 15. Morphology of the backbone, including neural and hemal spines in the posterior body
region of (A) the mackerel Scomheromorus mac‘ulatus and (B) the tuna Euthynnus allerteratus. Mack-
erel spines are slender and more angled posteriorly, whereas tuna spines are more robust and more
vertical, and have bony struts (arrow in B) that increase backbone stiffness. In (C) the wet backbone
of E. alletrerutus is bent, showing the tendency for the neural and hemal spines to extend out of the
plane of the vertical septum (arrows) in the absence of connective tissue fibers.
studies (Nursall, 1956; Fierstine and Walters, 1968) referred to the high stiffness
of the caudal peduncle of tunas. However, Hebrank (1982) found that stiffness
was lowest in the caudal region of skipjack where a flexible joint is present be-
tween vertebrae of the modified lateral keel.
The mechanical properties of whole backbones and intervertebral joints have
been measured in several scombroid taxa. The lateral stiffness of the backbone of
blue marlin (Makuiru nigricuns) is lower than that of scombrids (Hebrank et al.,
1990), suggesting that it is a more undulatory swimmer than tunas. Long (1992)
used dynamic bending tests to reveal the stiffness and damping properties of the
blue marlin backbone and used the mechanics of the intervertebral joints to cal-
culate the total work that a set of myomeres must do over the complete locomotor
cycle. Increased axial stiffness can also be achieved by contraction of axial mus-
culature (Long and Nipper, 1996), so that the waveform of the body of an undu-
latory swimmer is determined in part by the stiffness contributions of vertebral
column, myomeres, and the horizontal and vertical septa. There is a phylogenetic
trend from lower vertebral stiffness in billfishes and mackerels to increasing stiff-
ness in the tunas, suggesting the need for a broader survey of mechanical proper-
ties to integrate with other data on functional morphology.
In most fishes, the neural and hemal spines of adjacent vertebrae are tightly
bound by a set of collagen fibers to form the vertical septum (Figure 16). In scom-
broid fishes, the vertical septum is hypertrophied, with strong arrays of collagen,
and likely plays a role in force transmission and energy storage in locomotion.
Biomechanical models of the vertical septum developed at the BioDesign Studio
(Duke University) were presented at a conference on aquatic locomotion in Plym-
outh England (Wainwright, 1991). A mechanical model of the vertical septum
begins with the fact that the neural and hemal spines are angled posteriorly, ex-
tending rearward beyond the intervertebral joint (Figures 15A and 15B). This
morphology causes the distal portions of the neural and hemal spines to tend to-
ward rotation out of the vertical plane during bending (Figure 15C). However, a
woven fabric of collagen fibers binds the spines of adjacent vertebrae together,
preventing distal spine rotation out of the plane of the septum (Figure 16). The
collagen fiber matrix is a crossed-fiber array, in which the fibers are oriented in
two primary directions, ranging from 45’ to 55” to the vertebral axis (Figure 16C).
If the collagen fibers prevent motion of the spines out of the vertical plane, then
the spines will twist along their lengths.
Fig. 16. The vertical septum of the yellowfin tuna, Thunnus albacares. (A) Freshly dissected
backbone, including neural spines, hemal spines, and intact collagen fiber matrix of the vertical sep-
tum. (B) Vertical septum viewed through polarized light. Note the crossed-fiber array of collagen in
the vertical septum that binds the spines together. (C) Magnified view of highly oriented cross-fiber
array of collagen in the vertical septum. Fiber angles range from 45” to 55” for those that extend
upward and rearward. and 60” to 70” for those that course downward and rearward.
Physical models of this design showed strong strain energy storage under
bending (Wainwright, 1991), suggesting that strain energy may be stored in the
twisted neural and hemal spines and the crossed-fiber matrix during axial undu-
lation. Videler (1993) illustrated a strikingly similar model of the vertical septum,
but refers to septal fibers that run “primarily in one direction.” Collagen fibers in
vertebrate axial septa are rarely, if ever, organized in a single direction, highlight-
ing the need for use of polarized light in the examination of collagen fibers (Fig-
ure 16). Gemballa and Britz (1998) recently used this approach in a broader sur-
vey of intermuscular tendons in a diversity of fishes. Use of this technique and
study of freshly dissected backbones with the vertical septum intact in dynamic
vertebral bending tests (Long, 1992) will refine and test hypotheses of backbone
and vertical septum function.
X. SUMMARY AND FUTURE RESEARCH
The myomeres, the mechanical design of skeletal elements in backbone and

tail, and particularly the intricate design of axial connective tissues are key indi-
cators of pathways of force transfer during locomotion in mackerels and tunas.
Morphometric data on these structures, combined with physical models of the
anatomy, have produced several insights into the function of the locomotor sys-
tems of scombrid fishes. The main horizontal septum is formed by the conver-
gence of myosepta. One set of tendons in the septum, the POTS, collect the
longitudinal forces created by shortening of the myomeres and transmits them
posteriorly and medially to the backbone, where bending moments occur at the
intervertebral joints. The other set of tendons in the septum, the AOTs, resist ra-
dially expansive hydrostatic pressure, thus stiffening the anterior-pointing cones
and the skin. The AOTs thus supply tension to the slings that maintain the lateral
position of the POTS, giving POTS a large moment arm with which to bend the
backbone.
The model of force and velocity transmission by the POTS shows that the
geometry of the myosepta determine their ability to transmit force and motion to
the backbone. A steeply angled POT system, such as that of most mackerels,
transmits bending force to the backbone at the expense of displacement advantage.
Tunas, with their long POTS at a low angle to the vertebrae, transmit relatively
high velocity posteriorly from the anterior musculature to the tail. The second
model, that of the cone-shaped muscular hydrostat, demonstrates that the AOTs
are put into tension by the radial expansion of contracting muscle. This model,
based upon the relationships between dimensions and volume of cylinders and
cones, shows that the degree to which hydrostatic forces are used to put connective
tissues of the horizontal septum into tension depends upon the initial geometry of
the cones and the degree to which the cones change geometry during muscle con-
traction. The predictions regarding force transmission in both of these models

need to be tested through analyses of kinematics, mechanical properties of tissues,
internal pressure profiles, and patterns of muscle activity in the locomotor muscle.
The models we propose raise several questions about axial locomotor mor-
phology and force transmission. What is the effect of slow oxidative muscle po-
sition on locomotor biomechanics? The distribution of the aerobic red muscle
fibers within the myomere is of paramount importance to the long-range cruising
locomotion typical of scombrid fishes. Previous studies (e.g., Fierstine and Wal-
ters, 1968; Graham et al., 1983) found extensive variation in morphology and
position of red muscle in the myomeres of scombrids. The red muscle of mack-
erels that is positioned laterally will exert force primarily on the POTS to exert
force directly on the vertebrae. The red muscle of tunas also lies along the hori-
zontal septum and is connected to the POTS, but this internal muscle may also
function to exert radial tensile forces in the AOT through the hydrostatic cone
model. Recent analyses of the in vitro contractile properties of individual red
muscle fibers (Altringham and Block, 1997; Rome et al., 1992) and the motor
patterns of red muscle in swimming tunas (Shadwick et al., 1999) may contribute
the physiological data on muscular input that is necessary to test these models.
The mechanisms of caudal fin function in scombrids are of clear functional
relevance due to the high aspect ratio of the tail and the powerful thrust during
swimming for which these fishes are famous. The serially homologous myomeres
in the caudal region are modified to contribute to the great lateral tendon and the
medial caudal tendon for transmitting force to the tail (Figure 10). We suggest a
basic mechanical design for force transmission in the caudal fin that begins to
answer the question, how does the essentially separate mechanism involving the
posterior segments, caudal musculature, and the GLT interact with the more an-
terior mechanisms of backbone undulation? Further testing of a biomechanical
model of the caudal region may reveal how muscular forces are transferred
through the caudal tendons to the caudal fin during the power stroke. The vertical
septum is an additional functional complex in fishes that has received little atten-
tion but may play an important role in the biomechanics of aquatic locomotion.
A complete phylogenetic analysis of functional characters is not yet possible.
as we still need morphological and functional data sets for most taxa. However,
preliminary phylogenetic mapping of key locomotor characters (Figure 1) reveals
that a number of functional modifications occur at the transition from bonitos
(Sardini) to tunas (Thunnini). Thunniform locomotion (Figure 1, node F) is ac-
companied by a high-aspect-ratio caudal fin, fully internal red muscle, elongate
anterior-pointing cones, regional endothermy, long, low-angled posterior oblique
tendons, a fused hypural plate, a modified caudal keel with a flexible joint, and
reduction of the hypochordal longitudinalis muscle to a ligament. The functional
implications of longer cones and low-angled POTS can be explored using me-
chanical models proposed here, hut many of the unique features of tunas await
further experimental testing and comparison to other scombroid fishes. Also of

note is the apparent independent evolution in the billfishes and tunas of high-AR
caudal fins, long ARCS, and extremely heavy, cordlike systems of collagen in the
main horizontal septum.
In summary, the two major goals to strive for in future research are (1) a broad
comparative approach to locomotor morphology that will allow the integration of
mechanical models with the rapidly increasing knowledge of scombrid phylogeny
(Block et al., 1993; Block and Finnerty, 1994; Collette, 1978, 1997; Johnson,
1986) and (2) experimental testing of models of mechanical design of the myo-
meres, horizontal septa, vertical septum, and caudal tin in the context of research
on tuna behavior and physiology (Altringham and Block, 1997; Block, 1991;
Brill, 1987; Carey, 1981; Dewar and Graham, 1994; Graham et al., 1989; Shad-
wick et al., 1999). The locomotor mechanisms of scombrid fishes will only be
understood when we adopt an approach that combines information from phy-
logeny and physiology with the testing of mechanical models through measure-
ment of kinematics, muscular motor patterns, and the mechanical properties of
axial tissues.
ACKNOWLEDGMENTS
Many thanks to B. Block and D. Stevens for coordinating this volume and for their help with the
manuscript. Special thanks to J. W. Nursall for his insightful comments on the chapter. The ideas in
this chapter were aided and abetted in many ways by C. A. Pell, J. H. Long, Jr., and D. A. Pabst.
Funded by ONR Grant NOGO14-99-0184 and NSF Grant DEB-9815614 to M. W. Westneat.
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209-228.
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3,63-68.
Wainwright, S. A. (1983). To bend a ii&h. In “Fish Biomechanics” (Webb, P., and Weihs. D.. Ed\.).
pp. 68 -9 I. Praeger, New York.
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Nut. Sci. Philadelphia 125, 225 ~-3 17
8
SWIMMING AND MUSCLE FUNCTION

JOHN D. ALTRINGHAM
ROBERT E. SHAD WICK
1. Introduction
II. Swimming Performance
111. External Body Form
IV. Swimming Kinematics and Hydrodynamics
V. ~Muxk Structure and Physiology
VI. Endothermy
VII. Slow Muscle and SL[stained Swimming Performance
VIII. Muscle Function during Swimming
IX. Modeling Muscle Function
X. Force\ Generated hy the Muscle
Xl. Do Caudal Tendon< Function as Sprmgs!
XII. The Uncoupling of Slow Mu~lr Strain liom Body Bending
X111. Variation\ within Scomhrid\
XIV. Summary
XV. Directions for Future Research
Scombrids stand out from most other fish by their ability to cruise at relatively
high speeds and migrate long distances. This chapter briefly describes the mor-
phological adaptations that have equipped tuna for continuous, fast, efficient
swimming, and their unique body kinematics and hydrodynamics. The emphasis,
however. is on recent work on muscle function. The distribution of slow muscle
in the body, and the way in which it is used to generate thrust, can be seen as a
complex continuum in fish, and tuna lie at one extreme. Slow muscle in tunas is
concentrated near the midpoint of the body, and forms a large internal mass. In
each half tailbeat, rapid muscle activation on one side of the body leads to a brief
pulse of power generation that appears to be transmitted directly to the caudal fin
by the long posterior oblique tendons. This generates a strong vortex at the caudal
tin to provide thrust. Internalization of slow muscle and its concentration half way
along the body are seen in ectothermic scombrids and may have been a preadap-
tation for endothermy. The internal slow muscle oftuna shows signs of physiolog-
314 JOHN D. ALTRINGHAM AND ROBERT E. SHADWICK
ical adaptation for improved function at stable, elevated temperatures. To high-

light the ways in which tuna are similar or different to other fish, comparisons are
made wherever possible with other scombrids, and with nonscombrid fish.
I. INTRODUCTION
This chapter addresses the challenging problem of how tunas use their muscle
to swim. Tunas are high-speed pelagic predators that spend their entire lives swim-
ming. To sustain fast, continuous locomotion, tunas have evolved a suite of mor-
phological specializations that distinguish them from other fishes. Here we sum-
marize recent research on body kinematics and muscle mechanics of tunas and
other scombrids which has provided a quantitative basis for understanding the
unique features of thunniform swimming. To highlight the similarities and differ-
ences with other fishes, our discussion is put into context of data from other spe-
cies of scombrid and nonscombrid fish.
II. SWIMMING PERFORMANCE
In his 1978 review, John Magnuson noted that “scombrids are astounding
bundles of adaptations for efficient and rapid swimming. . . The entire biology
of scombrids is tightly linked to swimming as a way of life.” It is from this point
of view that we have begun to analyze the mechanical design and function of
locomotor muscle in these fish.
Scombrids stand out from most other fish by their ability to cruise at relatively
high speeds and migrate long distances. Most swim continuously at speeds rang-
ing from 0.33 BL s- ’ (body lengths per second) to over 2 BL s’, and few cruise
at less than 1 BL s’ (Magnuson, 1978). The slowest recorded species is the
wahoo, Acanthocybium solandri, which has an elongated body form unusual in
scombrids. Thunnus species are typically faster at about 1 BL ss’, and Euthynnus
often exceed 2 BL s .I. Large, mature specimens of Thunnus thynnus have high
absolute speeds, but are slower in terms of body lengths per second (0.3-l BL s-l;
Wardle et al., 1989). Against this trend, it should be said that species with the
fastest recorded cruising speeds include skipjack (Katsuwonus pelamis), bullet
mackerel (Auxis rochei), and Atlantic bonito (Sarda sardu). Cruising speed does
appear to be related to the presence or absence of a swim bladder. In general, the
more negatively buoyant species without swim bladders swim faster to generate
sufficient lift to avoid sinking. Speed is also inversely related to the area of the pec-
toral fins used to generate lift (Magnuson, 1978). Few nonscombrid teleosts are
continuous undulatory swimmers: exceptions include migrating salmon, which
can swim at speeds of 1-2 BL ss’ for several hundred kilometers (Johnson and
Groot, 1963: Neave, 1964; Beamish, 1978).
8. SWIMMING AND MUSCLE FUN(“I‘ION 315
Burst speeds in scombrids are less variable than sustained speed (Magnuson,
1978), ranging from 12 to 15 BL s I. The highest recorded speed was for Acon-
thocybium, which is not surprising given its elongated body. The high-speed, high-
efficiency “design” of tunas has led to compromises: they are much less maneu-
verable than most other fish (Blake et al., 1995). What are the important features
of this design? Tuna differ from other fish in their external and internal anatomy.
swimming kinematics, and physiology, and in the way their locomotor muscle
functions. Only recently have these properties been investigated quantitatively by
kinematic analyses of tunas swimming at steady speeds and by in vitro and in live
investigations of muscle dynamics.
III. EXTERNAL BODY FORM
There is a long-standing appreciation that scombrids, particularly the tunas.

have biomechanical specializations that give them superior swimming ability
among the teleosts (e.g., Lindsey. 1978; Magnuson, 1978). Indeed, some of these
features, such as the high-aspect-ratio lunate tail, streamlined body, elongate
myotomes, and internalized and endothermic slow muscle, are also found in the
fast-swimming lamnid sharks, and are generally considered to represent the most
highly evolved adaptations for efficient, and relatively fast, sustained swimming.
In terms of streamlining, the body thickness to length ratio is close to the opti-
mum for minimum drag (Hertel, 1966). Thunnus, Euthynnus, Kutsuwonus, and
Auxis could not be nearer the optimum, Surda and Scomber are very close, and
only Acunthocybium among species studied is too slender to have a minimum
drag : volume ratio. Flow over a body is likely to be laminar, even at high speeds,
up to the point when the body begins to taper toward the tail. The position of
maximum body thickness should therefore be well back on the body and in scom-
brids is around 0.4-0.5 BL from the snout. There are no significant differences
within the scombrids (Magnuson, 1978), but the position of maximum body thick-
ness in nonscombrids is generally further forward. The rounded body profile of
scombrids also increases swimming efficiency (Weihs, 1989). However. the body
is not circular in section, but ellipsoidal, to limit lateral movement of the body
(Lighthill, 1969). The narrow caudal peduncle reduces kinetic energy losses due
to movement of water (Lighthill, 1969). Lateral keels on the peduncle reduce tur-
bulence (Webb, 1975) and possibly provide some lift (Magnuson, 1970). Another
anatomical specialization in scombrids is the presence of finlets, small non-
retractable fins that occur in pairs along the dorsal and ventral midlines anterior
to the caudal tin. In tunas there are h--IO pairs. These appear to direct cross flow
between the two sides of the body toward the tail, which may help to maintain
laminar flow over the tail and augment lift (Magnuson, 1970; Webb, 1975), pre-
vent boundary layer separation, and reduce drag (Lindsey, 1978), or even prevent
roll (Walters, 1962). In a kinematic study of finlets in the chub mackerel S~~omhc~r
316 JOHN I). ALTRINGHAM AND ROBERT E. SHADWTCK
Fig. 1. Vorticity enhancement hypothesis proposed by Nauen and Lauder (2000). (A) dorsal
view; (B) lateral view. In both views the tail is decelerating toward one lateral extreme position (large
arrow in A). A possible path of water flow is indicated by the small arrows. The water flowing over
the peduncle is directed into the developing vortex V2. adding to forward thrust (from Nauen and
Lauder, 2000, with permission from Company of Biologists, Ltd.).
japonicus, Nauen and Lauder (2000) proposed that water flow is directed longi-
tudinally along the keels as the tail fin is decelerating at the extreme of its lateral
stroke, thereby enhancing the development of a caudal fin vortex and the resulting
thrust (Figure 1).
Prominent scales are rarely found in tuna, but some species have a scaled zone
called the corselet just behind the operculum. It has been suggested that it may be
a drag reduction device: the corselet could prevent breakaway, by introducing
microturbulence to the boundary layer, thereby reducing the velocity gradient
(Walters, 1962). Webb (1975) suggests it serves as a fairing for the pectorals,
which are held against the side during burst swimming. The second dorsal fin also
fits into a slot during burst swimming, as do the pelvic and first dorsal fins, which
8. SWIMMING AND MUSC1.E Ft'N('iW~N 317
are only opened during maneuvering. The second dorsal and anal fins reduce lat-
eral body movement (Magnuson, 1978). The body is extremely smooth, even
around the eyes, opercula, and so on. Finally, the caudal (and pectoral) fins of
scombrids are typically lunate and have a high aspect ratio, both increasing the
lift: drag ratio (e.g., Lighthill, 1969). Aspect ratios of > IO for pectoral fins and up
to 8 for caudal fins in scombrids are the highest recorded in fish, although sailfish
and marlin are comparable. Thunnus, Euthynnus, Kutsuwonus, and Auxis have the
highest aspect ratios, and Scomber, Sat-da, and Acunthocybium some of the lowest.
although some Thunnus fall into the latter group (Magnuson, 1978).
IV. SWIMMING KINEMATICS

AND HYDRODYNAMICS
Swimming in tuna is characterized by minimal lateral movement of all but the

caudal region of the fish, and virtually all of the thrust comes from the caudal tin
(e.g., Lighthill, 1970, 1975). For theoretical reasons reviewed at length by Mag-
nuson (1978) the thunniform mode is believed to be a highly efficient way of
swimming, a view supported by the oxygen consumption measurements of Dewar
and Graham ( 1994a).
Breder’s ( 1926) classification of swimming modes is clearly an oversimplifi-
cation, but provides a useful framework. It places tuna at one end of a spectrum
of swimming styles, in the thunniform swimming mode. At the other end are the
anguilliform or eel-like swimmers that throw their entire body into a series of
large-amplitude waves and generate thrust along most of their length. This mode
is energetically inefficient and slow. Between these two extremes there is a con-
tinuum through subcarangiform to carangiform swimming, the latter grading into
thunniform. Within those species which swim using their body musculature there
are many species which do not fit into this series, for example, those designed for
acceleration or high maneuverability. and then there are the many species that
swim using paired and unpaired tins other than the caudal fin. We will confine our
discussion in this review to the main anguilliform to thunniform series, since this
allows us to describe tuna in relation to other fish without undue complexity.
Undulatory swimming is powered by a backward-traveling wave of body
bending that must push against the water to generate thrust. Since the water yields
as the fish pushes against it. the wave must travel backward faster (~1)than the fish
swims forward (u). The amplitude of the wave also increases as it travels down
the body, with the lateral displacement of the tail tip (peak-to-peak) generally
being about 0.2 BL in most species. The number of waves on the body at a given
instant varies between approximately 0.7 and 1.7 in different species (Videler,
1993; Wardle et al., 1995). Swimming speed, expressed in BL s ‘, is strongly
correlated with tailbeat frequency (TBF), but not tail tip amplitude. Speed in-
creases are driven by increases in the propagation of the activation wave along the
body, culminating in faster TBF and generally little increase in tail tip amplitude.
Thus, for steady swimming the kinematics are relatively constant in terms of tail-
beat period (Wardle and Videler, 1993; Wardle et al., 1995). Stride length, the
distance moved in a tail beat, varies from 0.4 to slightly > 1.OBL between species:
u/v increases (i.e., there is less slip) as stride length increases (Videler, 1993).
Stride length in tuna and other scombrids varies considerably and there are no
apparent trends within the scombrids (Table I) or between them and other species
(Videler and Hess, 1984; Wardle et al., 1989; Wardle and Videler, 1993; Dewar
and Graham, 1994b). Direct comparison is difficult because stride length varies
with swimming speed and size in many species. Table I does show, however, that
the highest stride lengths reported are for fish swimming unrestricted in large
tanks or at sea, rather than in flumes. Videler (1993) likens the maximum stride
length to the fish’s “top gear” when the fish is swimming at maximum speed.
Wardle and Videler (1980) proposed that the very high speeds in tunas may be
accomplished by stride lengths much greater than 1.0 BL, but so far there is no
evidence to support this model. It is probable that many of the published values
reflect suboptimal performance. We would predict tuna to have longer maximum
stride lengths and higher u/v values than most fish. However, since thrust is gen-
erated primarily at the tail, not by lateral motion of body segments, the ratio
of ulv may not be important as an indicator of efficiency.
A kinematic analysis of yellowfin tuna was conducted by Dewar and Graham
(1994b), who used video images of 32- to 53-cm-long fish during steady swim-
ming in a water tunnel treadmill at speeds up to 3 BL ss’. Their work described
the lateral movements of the body, the yaw of the head, and the relation between
swimming speed and TBF. They showed that the length-specific caudal amplitude
and stride length are similar to those of other teleosts, but that the relative increase
in TBF with increasing speed is less. For example, a TBF of 2 Hz was required to
swim at I BL ss’, but this increased to only 4 Hz for swimming at 3 BL SK’.This
situation probably occurs because the TBF is relatively high (and stride length
relatively low) at low speeds near the minimum sustainable for each species. This
might reflect a low swimming efficiency at the lowest speeds: the lift-based caudal
thrust mechanism may not be highly effective when the tail is not moving rapidly
through the water.
As mentioned above, the major kinematic feature in tunas that sets them apart
from other teleosts, and even other scombrids like mackerel, is that the lateral
excursions of the body are more limited to the tail region. Consequently, the am-
plitude envelope (a plot of the body wave amplitude as a function of axial posi-
tion) is narrow in the front and midbody, and rises more steeply toward the tail,
compared with other fish. Figure 2 shows such a comparison for a series of fish
from eel to tuna. At 0.5 BL the wave amplitude in tunas is only about 0.1 of the
amplitude measured at the trailing edge of the caudal fin, whereas the relative
amplitude is 0.17 in mackerel, 0.25 in the subcarangiform group, and 0.45 in the
Table I
(‘omparison of Swimming Speed (U). Tailbeat Frequency (1’). and Stride Length (L,) for Tunas and Other Scombrids
Water temp. Body length U .f L

Common name (“(3 Cm) (BL\ ‘) (Hz) WJ Method Source”
Atlantic mackerel 12 0.3 l-O.35 5.0-18 5.4-14.9 0.76-1.04 Tank 12-14

Chub mackerel 17-20 0.26-0.32 I.O-12.0 1.9-16 0.53 -0.75 Flume 7. x
Pacific bonito 27 0.57 I .5-4.0 I .x-s..5 0.72-0.83 Tank IO
20 0.6-0.7 0.9-2.4 1.2-3.2 0.75-0.79 Tank I.1
Atlantic bonito IX 0.16 3.75-0.25 6.0-9.0 O.h2-0.69 Flume II
Kawakaw>a 2s 0.4-0.6 3 I-82 7.014.0 0.42 -0.52 Tank 5
24 0.38 I.36 3.0 0.44 Flume 2
Albacore tuna I(>- 17 0.9 0.74-1.23 1.X6-2.1 I 0.4-0.58 Flume 6
Bluefin tuna 20 2.3 0.6-l .2 0.54-0.93 Sea pen IS
Yellowtin tunii 21.. 26 0.52 3.0-10.5 2.0-13.0 0.75-l .5 Open ocean Ifi
2-l-28 0.53 0.51-2.5 1.5-3.5 0.4 -0.75 Flume 3
22-27 0.4-0.44 1.1-2.5 I .9-3.6 0.57-0.7 Tank 9
18 0.56 I.01 1.52 0.67 Tank 1
24 0.56 0.93 1.66 0.56 Tank I
Skipjack tuna 24-26 0.57 3.0-10.0 3.0-2 I 0.57-1.2 Open ocean I6
24-28 0.5 I I-2.8 i--4.8 0.33%0.6 Flume 2
22-27 0.38-0.41 I s3.7 2.8-5.2 0.53-0.71 Flume 0
Source\- (1) Alrringham and Block. I X7: (2, Drwar. 1993: (3) Deuar and Graham. l994b: (41 Ellerhy er ul.. 2000: (5) Fierstine and Waiters. 1968: (6) Graham
w (I/.. 1989: (7) Hunter and Zw>rifel. 1971 : (8; Knt~ and Shaduick. 109X: (41 Knosrr da/.. 1999: ( IO) Magnu\on and Prescott. 1966; (I 1J Pyatetskil. 1970: ( 12) \:tdeler
,md He\\. 1983: ( 13) Wardle and He. 1988; I 1-f) Wardle and Vidrler. 1980: (15) Wardle rl trl., 1989: (16) Yuen. 1966.
320 JOHN I>. Al ,TRINGHAM AND ROBERT E. SHADWICK
1.0 -
0.9 -
0.8 -
0.7 -
0.6 -
0.5 -
0.4 -
0.3 -
0.2 -
0.1 -
0.0 -- --I-L.Ld 3 -L-L.-.-

0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0
axial position (BL)

Fig. 2. Body wave amplitude (normalized to the maximum amplitude at the tail tip) as a function
of axial position (BL) for a number of scombrid and nonscombrid fish during steady swimming. Poly-
nomial curves were fit to data for eel (D’Aoiit and Aerts, 1999), mackerel (Katz and Shadwick, 1998)
and a group of aubcarangiform swimmers consisting of bass (V Jayne and Lauder, 1993, cod (a
Videler and Wardle, 1978) saithe (0 Videler and Hess, 1983). muskie (O), and trout (0 Webb, 1978).
The tuna curve 1s tit to data for skipjack. Kar.sun~onus pelami.s. and yellowtin, Th~nnus albaccrres
(Knower, 1998), and the horizontal bar represents the longitudinal position of the bulk of the internal
slow muscle in those two species.
eel at the same axial location. In tunas, the body tapers fairly abruptly beyond
0.7 BL, and it is only in this posterior region where the body cross-sectional area
and red muscle mass are greatly reduced that the relative amplitude rises above
0.3. As stated above, increased speed in undulatory swimming is not generally
accompanied by a concomitant increase in tail tip amplitude. However, tunas may
differ in this regard. A comparison of skipjack tuna swimming at low and high
speeds, shown in Figure 3, suggests that the amplitude envelop may indeed be
altered in sprinting, with a much larger lateral displacement seen in the posterior
third of the body. Whether this kinematic change is seen only during acceleration
or also at high-speed steady swimming is unknown at present.
In fish that swim by undulation of the body and caudal fins, two main ap-
proaches to describing thrust generation have been taken. One can be described
8. SWIMMING AND MUSCI,E FI.!N(‘TION .zz I
as the bulk momentum or added-mass method. and the other a lift-based method
As the body bends, and the bends travel down the fish, the body and caudal fin
push against the water, increasing the momentum of the water traveling backward.
The reaction to this is an equal force pushing the fish forward (see, e.g., Webb.
1978). The bending of the body also generates vortices that pass down the body
and are shed by the caudal fin into the wake of the fish (Figure 4). This generates
a reverse Karman vortex street. The reaction to this street pushes the tish forward.
It has generally been argued that for most fish the bulk momentum method wah
the most appropriate description. and that only in thunniform swimmers wax ;I
lift-based, vortex wake approach appropriate. However, Triantafyllou ef trl. ( I99.?)
showed that the Strouhal numbers calculated for more than 10 fish species were
in the predicted range for maximum efficiency of thrust generation from a vortex
wake. The list includes fish as diverse as bream, bonito. cod, goldtish. shark. and
trout. The Strouhal number S’ris tieiined as
0.4 ,
fast,j’
Fig. 3. Lateral displacement of the body mldlinr (peak-twpeak). normalized to body length (BI*)
as a function of axial position for a slow-swimming (2. I BL 5 ‘) Kor.wworrus pelrrmi.s and a f&t-
swimming (8.2 BL s ‘) Euth~nnu.\ uffirzis. indicating possible kinematic differences. The tail tip arn-
plitude is 0.2 BL at the slow speed and 0. iX BI. at the fat speed Drawn from data in Fierstine and
Walters ( 1968) and Knower ( I YYX i
Fig. 4. Vortex structure around a mullet (Chrlon labrosus) swimming in a straight line at constant
speed. P and S are pressure and suction zones around convex and concave bends, respectively. The
arrows show the main flow directions. Based on Miiller ef al. (1997).
wheref is the tailbeat frequency, A is the wake width (approximates to tailbeat

amplitude), and U is the forward velocity. St is the ratio of unsteady to inertial
forces, and should be in the range 0.25 -0.35 for optimal thrust development. Mtil-
ler et al. (1997) showed that a carangiform swimmer, the mullet, Chelon lubrosus,
has a Strouhal number of 0.34 and generates a strong vortex wake (Figure 4).
Approximately one-third of the energy in the wake is generated by the anterior
two-thirds of the body. They suggest that the undulating pump mechanism (put
forward by Blickhan et al., 1992) generates a circulation on the body. This circu-
lation flows down the body, joining the bound vortex at the tail before being shed
as a free vortex. Wolfgang et al. (1999) suggest that fish control this body-
generated vorticity through body flexure and caudal fin movement to maximize
the useful energy released in the vortex wake, a view supported by Mtiller et al.
(1997). In the transition from carangiform to thunniform swimming, the impor-
tance of the body-generated vortex will diminish.
V. MUSCLE STRUCTURE AND PHYSIOLOGY
Axial muscle of fish is arranged into segmental myotomes which have a com-
plex three-dimensional structure (reviewed by Videler, 1993). The myotomes
form stacked cones in which the muscle fibers follow complex helical trajectories
from one myotome to the next down the body of the fish. Myotomal and fiber
arrangement follow broadly similar patterns in all fish, but there are major dif-
ferences between selachians and primitive teleosts on the one hand, and more
advance teleosts on the other (Alexander, 1969). Alexander proposed that this
8. SWIMMING AND MUSCIX FUNCTION 323
complex arrangement enabled all fibers across the body section to undergo similar
strains during body bending.
The axial muscle of fish can be divided into two major types, fast-twitch or
white muscle and slow-twitch or red muscle, which are typically anatomically
discrete. Some species have a thin layer of pink muscle, intermediate in properties
between the fast and slow muscle (see Johnston, 1981). On the basis of histologi-
cal and sometimes physiological studies, several other types have been identitied
(e.g., Bone, 1978; Johnston, 1981). Most of the myotomal muscle is fast and typi-
cally 90-100% of the fish cross-section at a given point, and the proportion of
slow muscle is related to the ecology of the fish: constantly swimming pelagic
species have more slow muscle than benthic species (Boddeke et al., 1959; Vide-
ler, 1993). As a percentage of body mass, scombrids are 4-13% slow muscle
(Graham et al., 1983), although five of the seven species studied were between 4
and 7%. The slow muscle in most fish is confined to a zone, triangular in cross
section, beneath the lateral line, and generally makes up an increasing proportion
of the body cross-section toward the tail (Videler, 1993). However, some species
have different distributions of slow muscle, the functional significance of which
is often not known. Differences in relative slow muscle mass between scombrids
are small, but the slow muscle is distributed differently. There is a tendency for
some of the slow muscle to be placed deeper in the body, between the lateral line
and the vertebral column. In those species which possess countercurrent heat ex-
changers to elevate slow muscle temperature, this internalized slow muscle com-
ponent may constitute more than 50% of the slow muscle (Figure 5). However.
even in ectothermic species such as the bonito, Sarda chiliensis, a significant pro-
portion of the slow muscle is deep in the body (Ellerby et al., 2000). Graham et N/.
( 1983) showed that as a percentage of cross-sectional area, slow muscle of Au.xis.
Euthynnus, Kutsuwonus, and Thunnus reached a maximum at 0.4-0.5 BL from
the snout, in contrast to S. chiliensis and Scomher japonicus, where it was maxi-
mal at 0.7 BL. They suggested that this large difference between ectothermic and
endothermic scombrids is related to differences in swimming mode. However, if
expressed in terms of absolute muscle cross-sectional area, Thunnus albacores,
S. chiliensis, Scomber scombrus (Ellerby et al., 2000), and S. japonicus (Shad-
wick et al., 1998) all have their slow muscle peak at 0.5 BL. The peak is broadest
in Scomber and narrowest in T. albacares. In nonscombrid species, slow muscle
mass shows a broader distribution along the body (Ellerby et al., 2000). This
suggests an increasing localization of the ma.jor power source as locomotion has
become more specialized in the scombrids.
Is there a functional significance to this shift? One possible rationale is as
follows. In fish that generate thrust along much of their body by means of undu-
latory waves, slow muscle must be present along much of their length to generate
the bending wave-the presumed ancestral, metameric muscle arrangement?
Evolution toward sustained, high-speed swimming, which uses only the caudal lin
0.37L 0.45L 0.54L 0.71L 0.37L 0.45L 0.54L 0.71L
8. SWIMMING AND MUSC1.E FC?4(‘TlON .%25
to generate thrust, would benefit l’rom several “design” changes in the pouer’
source. An increase in slow muscle mass would increase the available power, ah
seen in most scombrids. Mechanically this muscle would be best placed in the
midline, and thus internal to the existing slow muscle. Placing slow muscle closel
to the backbone reduces its mechanical advantage, but the long posterior oblique
tendons found in many scombrids, which make acute angles to the backbone in
tuna and bonito, compensate for this placement (Westneat et ul., 1993: Ellerby
et ul., 2000). Power transmission to the caudal fin in a thunniform swimmer would
be mechanically more efficient from a discrete source on either side of the body.
in the fish’s midline, pulling directly on the caudal fin through tendons (analogous
to cursorial, terrestrial vertebrates). This might explain the increasing localization
of slow muscle at 0.5 BL. The disadvantage of such an arrangement is the reduced
maneuverability evident in many scombrids: they are designed for fast, straight-
line swimming.
At the other end of the spectrum, in eel-like swimmers. the distributed ar-
rangement of slow muscle along the body, and the relatively slow backward-
traveling wave of activation. delivers thrust gradually during a large proportion of
each tailbeat cycle. In the evolution of thunniform swimming, thrust generation
has become more discontinuous, occurring as more or less discrete bursts twice in
each tailbeat. An increase in the electromyography (EMG) wave speed and a lo-
calization of the slow muscle around 0.5 BL (Ellerby rt [I/., 2000) will facilitate
the production of discrete power bursts. We will come back to this subject later.
Fast and slow muscle types in fish are not homogeneous. There is a longitu-
dinal slowing of the twitch from anterior to posterior in most species studied (e.g..
Wardle et ul., 1989; Altringham P[ (11..1993; Davies and Johnston, 1993: Davies
et &., 1995; Rome et al., 1993: Altringham and Ellerby, 1999). Altringham and
Block (1997) observed a similar trend in yellowfin tuna, 7: &~~~ares. They also
showed that twitch contraction time decreased with increasing depth into the slow
muscle. In some tuna (e.g., ?: L&LZCXI-~.S and Kutsurvonu.s pelarnis: Knower 6’1ui..
1999) many of the fibers in the superficial slow muscle mass take on the appcar-
ante of intermediate- or fast-twitch fibers, suggestin,0 an increase in contraction
dynamics toward the tail (Figure S). Confirmation is required from mechanical
experiments, but Knower (1998) found that posterior superficial “slow” muscle
in 7: albacares and K. pelumis was active only during burst swimming, suggesting
faster mechanics. The significance of‘ these regional differences in muscle prop-
erties is not understood.
VI. ENDOTHERMY
The development of a large slow muscle mass for increased mechanical power
may have been an important preadaptation for the evolution of endothermy (Gra-
ham and Dickson, 2000). Significant gains in muscle power can be obtained
through small increases in temperature (see below), and any adaptations that led
to retention of some of the significant heat generated by active muscle would have
a selective advantage.
The ability of tunas to maintain elevated internal slow muscle temperatures is
well documented (e.g., Carey and Teal, 1966; Carey et al., 1971; Graham, 1975;
Carey, 1981). Tunas have a higher proportion of slow-twitch, relative to fast-
twitch, myotomal muscle than other teleosts (Magnuson, 1978; Graham et al.,
1983). The heat generated by muscle contraction and metabolism is conserved by
the internalization of the aerobic muscle mass and the presence of a countercurrent
heat exchanger (the rete mirabilis) in the circulatory system, which reduce con-
ductive and convective heat loss at the gills and body surfaces. Tunas have a high
standard metabolic rate and numerous specializations associated with increased
oxygen delivery to the tissues and high metabolic demands (Brill, 1987, 1996;
Brill and Bushnell, this volume). In continuously swimming fish, internal muscle
temperature may be maintained up to 21°C above ambient water temperature
(bluefin tuna, Thunnus thynnus; Carey and Lawson, 1973). In Katsuwonus, slow-
twitch muscle temperatures are 12°C above ambient, and in other Thunnus species
the steady state muscle temperature elevation is 6°C or less (Dizon and Brill,
1979; Graham and Dickson, 1981; Holland et al., 1992). Heat retention mecha-
nisms in aerobic muscle are not unique to tuna, being found in other large, active
pelagic fish: lamnid sharks (Carey et al., 197 l), Alopiid sharks (Carey, 1981; Bone
and Chubb, 1983), blue sharks (Carey and Scharold, 1991), and swordfish (Carey,
1990). This suggests that there are strong selective pressures for warming the lo-
comotor muscles. It has been suggested (e.g., Carey and Teal, 1966) that this sys-
tem of regional endothermy has evolved to enhance the locomotory performance
of the fish by increasing muscle power output, and this was recently tested by
Altringham and Block (1997) in yellowfin tuna, Thunnus albacares. Figure 6A
compares the power output of isolated deep, slow muscle fibers at different tailbeat
frequencies and temperatures. In vivo muscle action was simulated by imposing
sinusoidal strains on the fibers and timing stimulation to maximize muscle power
output. This approach has been widely applied to fish swimming studies (for re-
view see Altringham and Ellerby, 1999) and in the case of tuna, conditions which
Fig. 6. Relative power versus frequency curves for (A) deep and (B) superficial slow fibers from
the yellowfin tuna, Thunnus albacares, and for (C) superficial slow fibers from the bonito, Sarda
chiliensis. From Altringham and Block (1997) with permission from Company of Biologists, Ltd.
1.4
1.2
z
‘5 0.6
Q
-E
0.4
0.2
0.0
0 I2 i 4 5 6 7 8 9 IO 11 12 13
frequency (Hz)
0.2 i
0 1 2 3 4 5 6 7 8 9 IO 11 12 13 14
frequency (Hz)
1.4
0.8
0 I 2 7 4 5 6 7 8 9 IO 11 12 13 14
frequency (HY)
328 JOHN I). ALTRINGHAM AND ROBERT E. SHADWICK
optimize power production have been shown to match in vim conditions (Shad-
wick et al., 1999). As predicted, increasing temperature increases muscle power
and the tailbeat frequency at which it is generated. This is perhaps not surprising
and the same pattern might be seen in most muscles. However, comparison with
more superficial slow fibers from the same species (Figure 6B), and with results
from the slow muscle of the ectothermic bonito, Sarda chiliensis (Figure 6C),
shows some revealing differences. Power output of deep slow muscle from ;I: al-
bacares was more dependent upon temperature than both other muscle types. In
deep 7: albacares fibers there was a progressive increase in temperature sensitivity
as temperature was lowered from 30 to 25°C (Qs = 1.3 l), 25 to 20°C (Q5 = 1.40),
and 20 to 15°C (QS = 1.84). There was also a progressive increase in temperature
sensitivity with increasing depth (three depths studied) in the slow muscle (de-
pending upon location and temperature, Q5 increased from 1.2 to 2.0). Finally,
performance of the deep muscle of 7: albacares did not deteriorate until tempera-
ture was raised to 35°C. Slow S. chiliensis muscle deteriorated above 25°C. The
obvious conclusion to be drawn is that the deep slow muscle of 7: albacares has
adapted to perform best at stable, elevated temperatures. Slow S. chiliensis muscle
is more typical of ectotbermic fish: it has a low temperature dependence but is
unstable at temperatures above those experienced in the wild.
The marked adaptation for optimal performance at high, stable temperatures
seen in 7: albacares deep slow muscle is perhaps a little surprising, given that this
species typically maintains deep slow muscle only 6°C above ambient water tem-
perature (Dizon and Brill, 1979). The thermal properties of the deep slow muscle
of bluefin tuna, 7: thgnnus, which can be maintained 9-21°C above ambient
(Carey and Lawson, 1973), should prove to be particularly interesting.
VII. SLOW MUSCLE AND SUSTAINED

SWIMMING PERFORMANCE
At 25°C Thunnus ulbucures slow muscle generates maximum power at a tail-

beat frequency of 5 Hz (Figure 6). Free swimming, cruising fish used a tailbeat
frequency of <2 Hz, as reported by Altringham and Block (1997). 7’hunnus al-
bacares thus have a substantial power reserve in their large slow muscle mass,
which is probably sufficient to power sustained swimming at speeds significantly
greater than those used during normal cruising. Sustained, higher speed, aerobic
cruising is thus possible using the more efficient slow muscle, without the need to
recruit less efficient fast muscle. During bursts of activity when feeding, tailbeat
frequency was >8 Hz, but when searching for food between these bursts, frequen-
cies around 3 Hz were used, at a swimming speed of about 2 BL s I. Altringham
and Block (1997) calculated that only about 50% of the slow muscle would be
required at this speed and the muscle would still be producing less than maximum
8. SWIMMING AND MUSCL.E EUN(“TION 329
power output. Block et nl. (1997), tracking small, wild 7: dhucare.s, noted that
speeds of up to 3.5 BL s-’ could be maintained for over an hour.
Sarda chiliensis slow muscle also produced maximum power at tailbeat ii-e-
quencies greater than those observed during steady cruising, and this species also
has a large slow muscle mass (Ellerby et ul., 2000), suggesting a substantial power
reserve in the slow muscle. Data are not yet available to indicate how significant
this reserve may be. Most nonscombrid fish have proportionally far less slo\c
muscle, and it is unlikely that slow muscle is able to power swimming at more
than the slowest speeds.
VIII. MUSCLE FUNCTION DURING SWIMMING
During swimming myotomal muscle is activated on alternate sides of the

body. Anterior muscle is activated first, and a wave of activation travels from head
to tail, typically faster than the wave of body bending travels. Slow, sustained
swimming in all fish is powered by slow-twitch. aerobic, red muscle. Contraction
kinetics of this slow muscle are too slow to generate useful work at high tailbeat
frequencies (e.g., Attringham and Johnston, 1990). and most fish possesstoo little
slow muscle to generate sufficient power for rapid swimming. Fast, glycolytic.
white muscle is therefore recruited as swimming speed increases (e.g., Bone rful.,
1978; Johnston and Moon, 1980) It yields maximum power at appropriate fre-
quencies and there is enough of it to meet the high power demands of fast
swimming (e.g., Altringham and Johnston, t 990). During fast starts and bursts of
high-speed swimming, it is believed that all of the fast myotomal muscle may be
recruited. Early studies on tuna (e.g., Kayner and Keenan, 1967) demonstrated
that, as in other fish, slow swimming was powered by slow muscle, while at high
speeds the fast fibers were recruited. However, neither these nor any studies since
have shed light on how different regions of the large slow muscle mass are re-
cruited with changing speed.
IX. MODELING MUSCLE FUNCTION
To understand how tuna use their muscle to generate thrust, and to understand
how they differ from other fish, we first need to describe patterns of muscle ac-
tivity in a range of fish in some detail. As stated earlier, undulatory swimming is
powered by a backward traveling wave of body bending, generated by myotomal
muscle contraction. The form this bending wave takes is determined by the ar-
rangement and properties of passive elements in the body, muscle properties and
activity patterns, and the interaction between the ti\h and the reactive forces of the
water. More detailed reviews can be found in Videler (1993), Wardle et al. (1995),
and Altringham and Ellerby ( 1999).
As data become available for more species, slow muscle activation patterns
can be seen to fall into a sequence that can be related to body form and swimming
mode (Wardle et al., 1995; Knower et czl., 1999; Altringham and Ellerby, 1999).
The main features of this sequence, which are independent of swimming speed,
are shown in Figure 7. It should be remembered that some fish studied have body
forms and swimming modes which vary somewhat from the pattern described, for
example, those built for rapid acceleration or extreme maneuverability, and these
are not discussed. The colored wedges show when muscle is activated on alternate
sides of the body during a tailbeat. The x-axis is time through this tailbeat, and the
y-axis position on the body. Let us start with anguilliform swimming, before pro-
gressing toward tuna. In anguilliform locomotion thrust is generated against the
water along much of the body length, for most of the tailbeat. To achieve this, the
body is thrown into almost two complete, large-amplitude waves by the muscle
activation pattern shown. At any given instant muscle is active on both sides of
the body, and myotomes near the head are activated before those near the tail on
the same side have been switched off. During the transition to thunniform swim-
ming (from top to bottom of Figure 7) through subcarangiform and carangiform
modes, muscle activity patterns change, leading to:
1. An increase in &, the wavelength of body bending (expressed as a propor-
tion of BL); that is, the number of bending waves on the body at any instant
decreases from 1.7 to < 1
2. A decrease in the duration of muscle activity on one side of the body, as a
proportion of the tailbeat period
3. A decrease in the overlap of activity of muscle at the head and tail of the
fish and of muscle activity on opposite sides of the body
This leads to a transition from a more prolonged production of thrust along most
of the body length in eels, to short, discrete bursts of thrust at the tail only, in tuna.
Fig. 7. Electromyography (EMG) patterns in the slow muscle of scombrid and nonscombrid fish
during steady swimming. Time (x-axis) is expressed in terms of tailbeat period (T). At 0.5 T the tail
crosses the swimming track and maximum thrust is generated at the caudal fin (vertical dotted lines).
Body position as a fraction of fork length (BL) is given by the y-axis. Virtually all of the slow muscle
is found between 0.25 and 0.8 BL. In the bonito and the two tuna species there is little or no slow
muscle anterior IO 0.3 BL, indicated by the dotted horizontal line. The green and red polygons show
when muscle on the two sides of the body is active. These patterns are independent of swimming
speed. Data are from deep slow muscle of the two tuna species and from superficial slow muscle of all
other species. Data for eel are from Gillis ( 1998); trout, Hammond et al. (1998); bass, Jayne and
Lauder (1995); saithe and mackerel, Wardle and Videler (1993): bonito. Ellerby et al. (2000); and
tuna, Knower et trl. (1999).
0.8
0.7
0.6
0.5
0.4
0.3
0.6 0.X 1.010 0.2 0.4 0.6
I I
0.6 0.X 1.0/o 0.2 0.4 0.6
” 0.6 0.8 1.010 0.2 0.4 0.6
0.6 0.X 1.010 0.2 0.4 0.6
0.6 0.8 I .0/o 0.2 0.4 0.6
0.6 0.8 I.010 0.2 0.4 0.6
0.6 0.X I .O"O 0.2 0.4 0.6

failbeat period (7‘)
In the eel the waves of muscle activation and deactivation travel at similar
speeds, so that the duration of muscle activity is similar along the body length.
Furthermore, the EMG wave is comparable in speed to, or only slightly faster
than, the wave of bending. Active muscle shortening therefore occurs during much
the same phase of the muscle strain cycle at all points on the body. Muscle is
activated late in the lengthening phase of the strain cycle, and generates force
primarily during shortening. This has been shown to maximize power output from
trout slow muscle (Hammond et al., 1998), and from many other muscles (e.g.,
Altringham and Johnston, 1990; Johnson and Johnston, 1991; Altringham et al.,
1993). It is likely therefore that the slow muscle of the eel is also producing close
to maximum power. This is consistent with slow muscle at all points along the
body operating in the same way to produce hydrodynamic thrust locally. In the
subcarangiform trout and largemouth bass (Micropterus salmoides) the body
again makes a significant contribution to thrust, but most is generated by the tail.
This is associated with a phase shift between EMG and strain cycles, and a change
in local muscle function, which is more pronounced in carangiform swimmers.
In the carangiform saithe (Pollachius virens) the wave of deactivation travels
more rapidly than that of activation so that anterior muscle is active for longer
than that near the tail. Muscle activity ceases simultaneously at all points on the
body (Wardle and Videler, 1993). The waves of muscle activation and deactivation
travel faster than the bending wave and the underlying muscle strain wave. Muscle
activation therefore occurs earlier in the muscle strain cycle in more caudal my-
otomes. To increase swimming efficiency and performance, carangiform fish
swim with a longer & of lower amplitude and generate most of their thrust at the
tail. The phase shift between muscle activation and the strain cycle may assist the
transmission of power to the caudal fin. In addition to generating net positive
power, myotomes near the tail appear to spend part of each tailbeat as power
transmitters, assisting passive elements in the transmission of power generated by
more anterior myotomes (Altringham et al., 1993; van Leeuwen, 1995; Wardle
et al., 1995; Altringham and Ellerby, 1999). In anguilliform swimmers, power-
generating and thrust-generating elements are not separated, but distributed along
the body. In subcarangiform swimmers, we see the beginnings of a separation into
an anterior power source and a caudal thrust generator, which is even more evident
in carangiform swimmers. As discussed above, relative to anguilliform swimmers,
slow muscle is increasingly concentrated around 0.5 BL.
The carangiform pattern is also seen in the slow muscle of Scomber scombrus,
which has similar swimming kinematics to P. virens. EMG/strain patterns suggest
it uses its muscle in a similar way. However, there are significant differences in the
way muscle functions within the scombrids (Wardle and Videler, 1993; Ellerby
et al., 2000; Knower et al., 1999). Before addressing these, we will compare the
other scombrids studied with the carat&form swimmers to show the ways in
which thunniform swimrning is uniquely different. Figure 7, which shows only
EMG patterns, suggests that differences between scombrids and /‘. ~,ir-ensare
small; however, one feature stands out. There is a near coincidence between the
end of muscle activity and peak thrust at the caudal fin in &~-da chi/ipII.si.s. Ktr-
tsuwonus pelamis, and Tlzurznu,s mlhrrurrrs. In carangiform and subcarangilbrm
swimmers, including S. sc~otnhtw. peak force lags muscle activity. Strrtlrr chilien-
.sis, K. pelumis, and 7: a1hacarr.s all differ from the carangiform swimmers in
another important respect: the phase shift between the EMG and muscle strain
cycles from anterior to posterior myotomes is small (Knower et (xl., 1999; Shad-
wick et al., 1999; Ellerby eful., 2000). Recent experiments suggest that this means
there is unlikely to be a significant change in muscle function along the body. ah
seen in P. virens and S. .sc-omhrs. The evidence comes from a combination ot
mechanical experiments on isolated muscle fibers and studies of swimming fish.
The in ~ivo relationship between strain and muscle activity is determined by
simultaneous EMG and sonomicrometry recording in fish swimming at various
steady speeds. Sonomicrometry is an ultrasonic technique for measuring instan-
taneous length changes between implanted pairs of piezoelectric crystals. At the
same time video images are collected in order to analyze the midline kinematics
in relation to muscle strain. These experiments have shown that the wave of
muscle shortening travels at approximately the same speed as the wave of slow
muscle activation (Shadwick ct ~1.. 1999; Ellerby et ul., 2000). The onset of EMG
activity precedes the onset of muscle shortening by 30-50” for muscle at all lo-
cations. EMG activity continues well into the period of muscle shortening. This
pattern is independent of swimming speed. Work loop studies on isolated muscle
from S. chiliensis, ‘I: alhuwrcs ( Altringham and Block, 1997). and K. pelatnis
(D. A. Syme and R. E. Shadwick. unpublished) have shown that under these in
\Cw operating conditions. slow rrtu\cle between 0.35 and 0.7 BL will produce
close to maximum power during \teady swimming. The power this muscle pro-
duces is probably transmitted directly to the caudal lin via the posterior oblique
tendons (POTS; Westneat et al., 1993). This probably explains the absence of a
lag between muscle activity and thrust at the caudal tin.
Coupling the results of sonomicrometry with body kinematics, Shadwick
et ~11.(1999) showed that in K. prhmis the minimum in muscle length at sites
along one side of the body corresponds closely to the time at which the tip of the
caudal fin reaches it greatest lateral deflection to that side. At 0.4 BL muscle short-
ening and tail tip displacement are virtually in phase, that is. the muscle shortening
on the left side begins when the tail tip is at its rightmost position (point b, Fig-
ure 8), and ends when the tail tip is at its leftmost position (point d, Figure 8). The
strain peaks are only slightly later at 0.7 BL. because the wave of muscle strain
travels caudally very rapidly.
JOHN D. ALTRINGHAM AND ROBERT E. SHADWICK
0.0 0.2 0.4 0.6 0.8

Time (s)
Fig. 8. Slow muscle strain at 0.4 BL (upper trace, solid) and lateral excursion of the tail tip (lower
trace) of a skipjack tuna swimming steadily at 2.1 BL ss’. Horizontal bars indicate EMG activity at
0.4 BL. Tail tip displacement to the right of the fish is positive. The four body outlines refer to points
a-d on the lower trace. The vertical bars on the outlines indicate 0.4 BL. (From Shadwick etal., 1999.)
The time course of caudal tendon force is indicated by the dashed curve, which was recorded in a
different experiment and superimposed with its time scale adjusted to match the cycle period and EMG
activity of the muscle length trace. (R. E. Shadwick. unpublished.)
X. FORCES GENERATED BY THE MUSCLE
By implanting buckle-type strain gauges on caudal tendons in Kutsuwonus

pelamis and Thunnus albacares, Knower et al. (1993, 1999) were able to record
muscle forces at various steady swimming speeds, as well as in a few bursts. These
8. SWlMMING AND MUSCLE FLJNCTION 335
records represent the summation of the internal force that is transmitted to the
caudal fin via the deep lateral tendons. While this does not account for forces in
the superficial tendons, the temporal patterns and relative changes are informative.
First, force begins to rise at EMG onset, while the muscle length is still increasing,
and peaks approximately as EMG activity ceases (see Figure 8). This coincides
with the tail tip crossing the swimming track, at the time when hydrodynamic
forces are likely to be maximal (e.g., Lighthill, 1969). Second, the rise of force is
slower than its decline after peaking, an indication that the tendon force waveform
represents a summation of force from the traveling contraction wave and the
more simultaneous deactivation along the body. Third. although the tendons ap-
pear to arise from myotomes of the posterior third of the body, the force in the
ipsilateral tendon begins to rise well before the activation has occurred that far
back. On average the force reached one-third of peak level when only the muscle
anterior of 0.65 BL was active (Knower, 1998). This observation demonstrates
that anterior muscle force is transmitted directly to the tail, likely via the complex
connective tissue framework (Westneat et al., 1993), and illustrates the basis of
thunniform swimming-that the anteriorly placed muscle mass drives the caudal
propeller directly.
Although there was some variability, tendon force generally showed only a
modest increase with speed over the range powered by slow muscle. However,
when fast muscle was activated during occasional bursts (TBF up to I6 Hz) tendon
forces typically rose IO-fold (Knower, 1998). consistent with a nearly 10: 1 ratio
of fast to slow muscle.
XI. DO CAUDAL TENDONS FUNCTION

AS SPRINGS?
The combination of in vivr~force data and the mechanical behavior of the

tendons makes it possible to assessthe potential function of the caudal tendons as
energy-saving springs in swimming. These tendons are robust collagenous struc-
tures that resemble tendons found in other vertebrates. Shadwick et ul. ( 1992) and
Knower (1998) subjected excised caudal tendons of Kutsuwonus pelamis and
Thunnus albacares to load cycling and determined that the modulus of elasticity
and energy dissipation ranged from 0.65 to 1.2 GPa and 7 to 25%, respectively.
when loaded to stresses that encompass the in vivo range. These compare closely
to the properties of mammalian leg tendons that are known to function as effective
biological springs in terrestrial locomotion. Knower (1998) performed postmor-
tem tensile tests on tendons from the same fish that furnished in vivo force records.
and showed that peak tendon forces during steady swimming could impose strains
of much less than 1% of tendon length, because the tendons are very thick. Even
the maximal burst forces recorded produced strains of only I .5-2% of tendon
length. Consequently, the strain energy stored in the stretched tendon is insignifi-
cant compared to the work done by the muscle in producing thrust. Thus, the
caudal tendons in tunas do not function as energy-saving springs, even at maximal
swimming effort. This conclusion is based on the following argument (Knower,
1998; Knower and Shadwick, in preparation). The net cost of transport deter-
mined for similar size fish (I .6 J BL- ’ ; Dewar and Graham, 1994a,b) was multi-
plied by speed in BL s- ’ to yield an estimate, in J s I, of the metabolic power input
required to swim. Assuming a metabolic efficiency of 25%, power input was con-
verted to muscle power output, which is also the power input to the caudal pro-
peller (Webb, 1975). Multiplying by half the duration of the tailbeat cycle gave an
estimate, in joules, of the mechanical work performed per tail sweep. A compari-
son of this quantity with the energy used to stretch the caudal tendons on one side
during a tail sweep revealed that tendon strain energy accounted for less than 0.5%
of the total mechanical energy used to swim. Even if this proportion rose by an
order of magnitude during burst swimming, the tendon strain energy would still
not be a significant factor in overall locomotor energetics.
XII. THE UNCOUPLING OF SLOW MUSCLE

STRAIN FROM BODY BENDING
Another distinguishing feature of tunas is the uncoupling of slow muscle

strain from local body bending. Unlike contraction of the superficial slow muscle
in other fish, the shortening of deep slow muscle in tuna significantly lags behind
changes in the local midline curvature (Shadwick et al., 1999; S. L. Katz and R. E.
Shadwick, unpublished). Analysis of midline curvature in Kutsuwonuspelumis as
a function of time showed that. at axial locations between 0.4 and 0.74 BL (where
the majority of the slow muscle mass is located), the wave of midline curvature
travels along the body in advance of the wave of muscle shortening (Figure 9).
In K. pelamis and probably other tunas such as Thunnus albacares (S. L. Katz
and R. E. Shadwick, unpublished), the temporal separation of slow muscle strain
and local curvature is so pronounced that, in the midbody region, muscle short-
ening at each location is synchronous with midline curvature at locations that
are 9-10 vertebral segments more posterior. Interestingly, this distance closely
matches the span of the elongated myotomes (Fierstine and Walters, 1968) and
these observations suggest that slow muscle contractions cause deformation of the
body at more posterior locations, rather than locally. This arrangement is quite
different from the bending beam model of slow muscle strain in other fish (van
Leeuwen et al., 1990; Coughlin et al., 1996; Katz et ul., 1999), but is consistent
with the hypothesis that tunas produce thrust by motion of the caudal fin rather
than by body undulations (Fierstine and Walters, 1968; Lighthill, 1970). Can
muscle shortening be uncoupled from local bending? It seems likely that forces
8. SWIMMING AND MUSC’I.F. l-3 i?r( IION
00 02 04 0.6 0.8
0 05 /-.. I 0.63BI -_ I __ ,--,
00 02 a.1 0.6 0.8 I .o
Time (s)
Fig. 9. Uncoupling of muscle strain front local body curwturc. CA) Muscle segment length. mea-
sured by ronomicrometry (in mm). on the Irft Gde of the body at 0.4 HL in a skipjack tuna swimming
at 2. I BL s ’ compared with tnidline cur\atuw tm cm ‘) at that same location and at a more posteriol
location of ().%I BL. (B) Muscle wgment length on the left side of the body at 0.63 BL III a skipjack
swimming at I .7S BL s ’ compared with curvature at 0.63 and 0.X2 BL. Positive values of curvature
indicate the midline i\ convc.x on the left. AIICW\ show the peak\ in mwcle length coincide with peak\
m convey curvature at more posterior location\ cfrom Shadwich 1’1 01.. Ic)W) with permission from
Company of Bi<>lo~i\t3. I td
and shortening generated by fibers in tish myotomal cones are transmitted along
the backbone through a network of myoseptal and dermal connective tissues
(Wainwright, 1983; Westneat et d., 1993: Westneat, this volume). In tunas the
contraction of internal slow muscle may project caudally through the posterior
oblique tendons that lie within the horizontal septum, the myoseptal connections
to the skin. and the robust tendons that link directly onto the caudal fin rays (Fier-
stine and Walters, 1968). Thus, local shortening could cause bending at more pos-
terior locations, and the slow muscle mass, while primarily located in midbody
regions. would function as a t’orceful actuator to deliver contractile power to the
caudal region. If correct. then shearing must occur between the internal slow
muscle and the surrounding mass of fast muscle which, when inactive, must de-
form in synchrony with the bending midline (Katz et al., 1999). How this may
change when the fast muscle actively shortens in fast swimming is not yet known.
Studies of fast muscle function in burst swimming remain a challenging goal of
tuna biomechanics research.
XIII. VARIATIONS WITHIN SCOMBRIDS
Scomber scombrus is a carangiform swimmer (Wardle and Videler, 1993).

Sarda chiliensis has swimming kinematics similar to those of S. scombrus (El-
lerby et al., 2000), but as a close ectothermic relative of the endothermic tuna, has
some features in common with them. Overlap between myotomal cones and the
lengths of the POTS of S. chiliensis are greater than those in S. scombrus and more
comparable to those of Katsuwonus pelamis and Thunnus albacares. Sarda chi-
liensis also has more slow muscle than S. scombrus, and a significant component
is internalized. Together with the small EMG/strain phase shift along the body,
these anatomical similarities suggest that S. chitiensis uses its muscle and POTS
in a similar way to tuna. However, unlike in tuna, deep muscle strain in S. chilien-
sis appears to be in phase with local bending, further emphasizing its status as a
possible transitional stage between carangiform and thunniform swimming. The
basic EMG pattern in all scombrids (Figure 7) resembles that of the carangiform
saithe. A rapid wave of EMG onset travels down the body, followed by a more
rapid wave of EMG offset, such that the proportion of the tailbeat during which
the muscle is active (the duty cycle) decreases from anterior to posterior. EMG
onset and offset wave speeds are greatest in 7Yalbacares, and in combination with
the greatest concentration of slow muscle around 0.5 BL and the largest A,,, make
muscle power production a more “pulsatile” event.
XIV. SUMMARY
In summary, in the endothermic tuna, and in Sarda chiliensis, muscle is active

only on one side of the body at any instant and it has a short duty cycle. This is
due to the progression of a rapid wave of muscle activation down the body and the
concentration of the slow muscle around 0.5 BL. Internal slow muscle at all lo-
cations operates under conditions which generate maximum power: there is no
apparent change in muscle function along the body. This power is transmitted
rapidly and efficiently to the caudal fin by the POT tendons. Power generation is
brief and maximal at the caudal fin just as slow muscle at all locations is switched
off. This mechanism yields the features that are the hallmark of “thunniform”
locomotion, namely, a low-amplitude body wave and powerful lateral undulations
8. SWIMMING AND MUSCLE FUNCT‘ION 339
of the thrust-producing lunate caudal hydrofoil. There is always a price to pay:

subcarangiform and carangiform fish are capable of rapid and complex maneu-
vers. In tuna, maneuverability has been sacrificed for a more efficient thrust gen-
eration mechanism.
XV. DIRECTIONS FOR FUTURE RESEARCH
Our current knowledge of anatomical design, muscle function, and swimming

mechanics indicates that tunas represent an extreme in undulatory swimming per-
formance. However, there remain many intriguing problems to resolve.
I. Scale effects. Tunas can grow to very large sizes, but most research so far
has been on relatively small and immature individuals. Wardle et al. (1989)
showed that fast muscle twitch time increases with body size in bluefin tuna,
indicating that maximal tailbeat frequencies decrease accordingly. Our
knowledge of how increasing body size influences swimming kinematics,
energetics, muscle mechanics, and preferred and minimum speeds is mea-
ger, but is essential for a compete understanding of the swimming perfor-
mance of the large, mature tunas that constitute the breeding populations.
2. High-speed swimming. We know very little about kinematics of high-
speed and burst swimming, and virtually nothing about the mechanics of
the fast muscle fibers that power it. Does muscle strain increase to power
high-speed sprinting, and is this reflected in an increase in tail tip ampli-
tude? At what speeds are fast fibers recruited, and what contribution, if any,
does the slow muscle make to burst swimming? What are the energetic
costs associated with maximal swimming performance?
3. Spatial activation of myotomes. It remains unknown whether muscle fibers
are activated sequentially according to their axial location or according to
the myotome they are part of, and whether activation patterns differ be-
tween fast and slow muscle. This issue is potentially very significant in
tunas where the highly elongate myotomes can span 13 or more vertebrae,
and a cross-section at midbody locations can contain fibers from an equiva-
lent number of myotomes.
4. Regional variation in muscle contractile properties. More experimental
evidence is needed to document the variations in muscle contraction speeds
which may occur within the slow and fast muscle as a function of axial
position, and also with depth at a given position. In addition, the role of
superficial slow fibers is unclear. Do they shorten in phase with the under-
lying slow fibers or in phase with local curvature’? At what speeds are they
active, and do these fibers have a longitudinal gradient in contractile prop-
erties’? Wardle et crl. i 1989) predicted that if top sprint speeds are set by the
twitch time of the faster anterior white muscle, then the cycle frequency
will be too fast for the slower posterior white muscle to follow and oppos-
ing muscles near the tail will overlap in their contractions. This could
contribute a stiffening effect and enhance force transmission in the caudal
region. Understanding the biomechanical function of these regional varia-
tions in muscle properties will be a major challenge.
5. Fluid mechanics and mechanical power. There are no direct measurements
of external forces or power output in a swimming fish. Estimates may be
made from visualization of fluid flow over the body and in the wake (e.g.,
Mtiller et al., 1997; Wolfgang et al., 1999). This type of approach could
make possible the calculation of mechanical power production and effi-
ciency in a swimming tuna and, in turn, allow interspecies comparisons, as
well as shed light on the importance of the finlets.
6. Internal force production and transmission. We have measurements of ten-
sile forces in caudal tendons and muscle strain along the body, but these do
not represent the pattern of force and displacement produced by any single
muscle fiber or fascicle. Thus we do not have the equivalent of an in viva
muscle work loop as has been obtained in terrestrial vertebrates and birds
(Biewener, 1998). This may prove to be an intractable problem, due to the
unusual muscle anatomy in fish, but the use of micro force transducers on
individual oblique tendons may prove feasible. This could provide infor-
mation on how the wave of muscle force travels along the body, and how
it is focused to the caudal tendons. Finally, the role of the skin in force
transmission needs to be addressed experimentally.
7. Interspecies comparisons. Evidence from anatomy, swimming mechanics,
and muscle activation suggests there are subtle differences between skip-
jack and yellowfin tuna slow muscle function (Knower et al., 1999). It
would be interesting to determine how these differences are related to
differences in their muscle contractile properties. Do differences in fast
muscle properties also exist, and what is the functional relevance? In a
broader sense, how does the biomechanical design of tunas compare to that
of other fast scombrids such as Acmthmyhium’?
8. Convergence with lamnid sharks. Pelagic sharks of the family Lamnidae,
such as the mako and great white, share several morphological features
with tunas that suggest they are adapted for fast, efficient swimming. They
are also able to conserve metabolic heat from their internal slow muscle
through the use of a countercurrent heat exchanger (Carey et al., 1971).
The evolutionary convergence of these two groups is intriguing because
they have evolved independently for over 400 million years. A detailed
study of lamnid swimming physiology and biomechanics in the context of
convergence with tunas represents a challenging venture for the future.
8. SWIMMING AND MUSCLE FUNCTION 341
ACKNOWLEDGMENTS
J.D.A. thanks David Ellerby for many useful discussions and the BBSRC for financial support.
R.E.S. thanks Stephen Katz and Douglas Syme for stimulating collaborations, and the National Sci-
ence Foundation for financial support
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TUNA OCEANOGRAPHY-AN APPLIED SCIENCE
GARY D. SHARP
I. Introduction
II. Historical Tuna Fisheries and Related Oceanography
A. Longlining-Wide and Deep Studies
B. Local Weather and Global Climate Change
III. Physics, Fisheries, and Dynamic Perspectives
A. Physical Structures versus Other Contextual Changes
B. Continuous Changes in the Big Picture
C. Changes in Markets and Resource Ownership
IV. A Brief Review of High Seas Tuna Fisheries Development Patterns
A. Innovations in Technology Play Major Roles in Recent Changes
B. Pole-and-Line Baitboats
C. Purse Seines
D. Longline Fishing Pattern Changes
E. Ongoing Changes in Longline Fleets and Fisheries Interactions
E Ocean Climate Changes and Fishery Responses
G. Disappearing Traditional Fisheries
V. Habits and Habitats of Tunas
VI. Coordinated Empirical Studies of Tuna Behavior and Abundance within Ocean Gradients
VII. Tuna Schools and Dynamic Interactions
A. Why Tunas Aggregate
VIII. The Importance of Studying Individual Fish Behavior
IX. The Ecocosmological Question: “Why Are Tunas Where They Are‘?”
X. Conclusions
I. INTRODUCTION
Empirical science and application are one in the field of tuna oceanography.
The observations from fishing vessels and decades of study from various ocean-
ographic platforms have proven of great value to understanding the relationships
between ocean variations and fisheries operations (Uda, 1927, 1957; Matsumoto
et al., 1960; Hela and Laevastu, 197 1; Saito, 1973, 1975; Saito and Sasaki, 1975;
345
Tuna Volumr 19
FISH PHYSIOLOGY
346 GARY D. SHARP
Sharp, 1978, 1979; Sund er al., 1981; Marsac and Hallier, 1991; Gauldie and
Sharp, 1995; Lehodey et al., 1997, 1998).
There are several major functions that tuna oceanography studies can provide
for those working to understand tuna fisheries and related tuna biology. One is to
help understand the variations of catch statistics from various fisheries operating
within similar or adjacent regions on one or more species of tunas. Another is to
help understand the general shifts in apparent population abundances over large
and small areas in time. Others include learning more about the responses of tunas
to ocean variability and production patterns so that forecasts of behaviors, catch
potentials, and status of resource population might be improved. The following is
a brief survey of recent and past efforts to improve our understanding and use of
fisheries and ocean data.
We have known from fisheries catch data, and recent decades of associated
satellite imagery, that tunas tend to aggregate about ocean features and disconti-
nuities (Sharp, 1976, 1978; Laurs and Lynn, 1977; Laurs (1997); Gunn and Block,
this volume). The recent ECOTAP research points clearly to the production and
feeding regime as the principle attraction to these features in horizontal and ver-
tical dimensions. We also know that much of the offshore, open ocean is more
structured vertically than horizontally, providing subsurface features and topog-
raphy that likely act as both “fueling stations” and “roadways” in this otherwise
relatively featureless environment. Major predators such as the tunas have cer-
tainly learned to take advantage of these cues and phenomena in order to thrive as
well as they do, particularly in the major ocean gyres, often described as being
hypertrophic, or “sterile.” Lest anyone doubt this, a quick examination of the
Atlas of Tropical Tuna Fisheries (Fonteneau, 1997) will show that there are few
or no oceanic regions between 45”N and 45”s that do not have substantial tuna
catches, depending upon the season. This is direct evidence that our abilities to
measure primary production, and hence ocean ecosystem productivity, are seri-
ously flawed and lead to underestimation of true ocean production levels through
the application of regionally integrated mean seasonal values. Recent studies by
Nicholas Welschmeyer of Moss Landing Marine Laboratories have confirmed that
conventional (C14) methods for measuring primary production underestimate
true production from 1.7 to 2.0 times on a transect from Monterey Bay to Hawaii
(Welschmeyer et al., 1999).
The two major reproduction and juvenile growout regions in the Atlantic for
several tuna species are the Sargasso Sea, southward toward the equator, and south
of the equator into the South Atlantic central gyre (Bard, 1981). The maturing and
mature adults appear to congregate seasonally along the western coastal rises, as
the short winter and spring blooms and subsequent peak production occurs, fol-
lowing the cascade of sequential higher trophic feeding. Offshore, the production
of the North Atlantic Subtropical region (NASTW, per Longhurst, 1995) peaks
and phytoplankton accumulates from November, peaks in April, and then declines
steadily until June, after which it is low until the cycle begins again. Feed for tunas
Fig. 1. Historical Atlantic bluefin tuna fisheries data, and the tag and release data from the re-
views by Mather et al. (1995) and Rivas (1978) along with recent PSAT and archival tag studies
provided the information to overlay onto the Longhurst (1995) monthly peak primary production maps
for the well-studied North Atlantic Ocean. Three known spawning areas of Atlantic bluefin tuna are
identified in the Gulf of Mexico-Caribbean Sea; the northern Mediterranean; and the Black Sea (where
spawners have been excluded for more than a decade due to massive ecosystem degradations). I have
attempted to outline the pathways from and to these spawning areas for adults, linked by feeding
grounds over the annual cycle, with at least one pattern from each of the east-west extremes, bifur-
cated by the warm Gulf Stream, and the very distinct production patterns north and south of it. An
important message is that the distances in the northern sectors are much less than those nearer the
equator. This suggests that seasonal east-west mixing of tunas from either the Gulf of Mexico or the
Mediterranean would be quite likely in the northern region, although true extents and any distinctive
behaviors have been elusive. We are learning quickly from new electronic tagging tools.
348 GARY D. SHARP
will increase with time after the initial blooms. To the north, in the North Atlantic
Drift (NADR) and Southern Arctic (SARC) domains, production peaks from June
through August as the pycnocline shoals and is fully illuminated, creating large
expanses of productivity extending across the North Atlantic from the Bahamas,
crossing the Azores, to Norway. Known Atlantic bluefin distribution and seasonal
production patterns are linked in Figure 1. These seasonal shifts in oceanic re-
gional production, and their spatial extents, likely explain the pattern of the blue-
fin tuna seasonal aggregation and dispersal found in the archival tagging studies
(Gunn and Block, this volume).
Similarly, the cold-tolerant southern bluefin tuna reproduces during the fourth
quarter and early first (summer) quarter in a region of the deepest tropical Indian
Ocean off northwestern Australia. This is when and where the surface water is a
combination of strongest Pacific Warm Pool flow-through from the Indonesian
archipelagos and convergent Indian Ocean gyre circulation (Verschell &al., 1995)
as functions of variable seasonal winds. Certainly the mix of the two produces a
situation that enhances both chemistry and nutrients, seasonally, to produce the
right milieu for the young bluefin tuna larvae to thrive, or not. The southern blue-
fin’s somewhat erratic recruitment success, like all the other bluefin tunas, is likely
a function of this production cycle, and their adult age structure variations as well.
The importance and impacts of local versus ocean domain production on
bluefin or other tunas with tendencies for localized, seasonal reproduction cannot
be overemphasized. Although all tunas appear to be capable of serial spawning,
those with longer, slower developing life-history strategies have had opened to
them the higher levels of subtropical to subarctic ocean production, with its gen-
erally lesser competition and stronger seasonal cycling. Their large adult sizes and
lesser ability to cope with tropical upper ocean metabolic demands shorten their
residence times in the already crowded upper tropical ocean domains. These won-
derful fishes’ unique adaptations and yet overlapping pathways point to how the
temperate-tolerant tunas and more tropical species have adapted via such different
strategies and capabilities. All these interactions are reflected in the rapidly evolv-
ing global tuna fisheries. The remainder of this chapter will deal with the suc-
cesses and types of questions that applications of multidisciplinary research and
the power of the new pop-off satellite tags (PSATs) can address and what they
cannot yet resolve.
II. HISTORICAL TUNA FISHERIES

AND RELATED OCEANOGRAPHY
In order to best understand what has already been learned about tuna ocean-
ography, it helps to understand a bit of the history of fisheries-tuna interactions
from localized, historical perspectives. Most modern tuna fisheries started from
9. TUNA OCEANOGRAPHY-AN APPLIED SCIENCE 349
coastal hook-and-line fishing centers, and expanded with migrants from these lo-
cations. The species of tunas caught were associated with either cool subtropical
habitats, for example, albacore and bluefin tunas, or the tropical yellowfin and
skipjack tunas. For example, southern California’s early 19th century pole-and-
line and troll tuna fisheries derived from applications of immigrant Okinawan fish-
ermen’s traditional technology and their counterparts from Sicily, the Azores, and
Madeira, where harpoons, seines, handlines, and trolled jigs were more tradi-
tional. West Africa’s industrial tropical tuna fisheries evolved first from Cape
Verde’s pole-and-line styles, and then those of Japanese joint ventures. These were
eventually joined by both Spanish and French high seas seining, that were in turn
cloned from southern California’s hybrid cultural fisheries developments. Bard
and Santiago (1998) review the historical surface albacore fisheries of the Atlantic
Ocean. Laurs and Lynn (1977) describe the affinities of subadult albacore for vari-
ous subtropical habitats, and their submergence as they mature and return to tropi-
cal latitudes.
The dynamic features that create major tropical tuna surface fisheries vary.
The environmental features that bind the eastern tropical Atlantic and Pacific are
the regions’ shallow oxygen minima as a result of seasonal winds and upwelling
production. More oceanic and island tuna fisheries are created by island wakes
and Taylor columns over sea mounts (Bakun, 1996), as well as by convergence
and divergence of ocean currents. Each unique fishery situation is caused by local
food-fish production. Dynamic local oceanography and the sequential cascades
of ecological production favor tropical tunas, particulaly skipjack and yellowfin,
whose nomadic upper-ocean lifestyles benefit from the minimal competition from
other tuna species or other large-sized predator fishes. Why? In the eastern tropical
Atlantic and Pacific fisheries, skipjack and yellowfin tunas dominate because the
higher productivity typically uses up the available oxygen during the night, and
below the photic zone, leaving too little oxygen (as we will explore next) at the
other tuna species’ preferred habitat depths and temperatures. Thus, the adults of
these other species are excluded from all but the very fringes of these vast eastern
tropical regions.
Surface-oriented skipjack and yellowfin schools dominate oceanic island sur-
face fisheries. In the upper ocean, where adequate oxygen levels are met, the tropi-
cal tunas coexist, but as oxygen levels decline, the smaller tunas’ requirements act
quickly to exclude them, while the lesser demands of older and larger tunas allow
them to swim and explore the lower oxygen levels (Sharp, 1978; Brill, 1994).
When oxygen levels reach thresholds between 3.5 and 2.0 ml/liter, most of the
tunas are excluded. Despite this limitation, deep thermoclines and scattered pro-
duction centers draw the larger, cooler-ocean-capable adult albacore and bigeye
into the depths, where they tend to scatter, minimizing competition among species
and within their own species. Development of oceanic longline fishing technolo-
gies was based on these scattered. deep distributions. These adults then find them-
350 GARY D. SHARP
selves orienting to physical-chemical gradients and interfaces and their resulting

ecological features, and become vulnerable to handline or longline fishers near
islands, sea mounts, and banks, particularly at night. The dynamics of the organ-
isms that form the deep scattering layer are key to this diurnal behavior (Sund
et al., 1981; Bertrand et al., 1999a,b).
A. Longlining-Wide and Deep Studies
It is from early studies of longline fisheries by Japanese scientists that we first

learned about the relations between ocean properties and the various tuna and
billfish species. It was while reading Hanamoto’s (1974, 1975) and Saito’s descrip-
tions of catches of tunas using vertical longlines that I decided we knew very little
or nothing about adult tuna behavior, distributions, or real abundances. The clue
came when after several research cruises using and improving vertical longline
gear (Saito, 1973; Saito and Sasaki, 1975; Hanamoto, 1975), they reported the
species counts by hook position/depth for their many fishing ventures into the
tropical central Pacific Ocean where all the Pacific tuna species were known to
coexist somewhere within the water column.
Although often caught, skipjack are rarer than other tunas on longlines, and
catches usually peak near the surface. Yellowfin were abundant, and peak catches
of adults occurred at about 125 m. They were not often caught below 250 m.
Albacore were next, caught below the smaller surface-oriented yellowfin, and
most often among the first bigeye, peaking at about 200 m or so. Then came the
new insight: bigeye catch rates (fish per available hook at each depth) were ob-
served to increase continuously from first depths of encounters to the bottom of
the lines, or to wherever available oxygen levels fell below 1 ml/liter, whichever
came first. The experimenters could not sink even these “improved” vertical long-
lines far enough into the ocean to reach the peak abundance of bigeye tuna. It was
clear that we had almost no idea where these tuna, and their more cold-tolerant
cousins, the bluefin tunas, could live, or actually thrived in greatest abundance.
Block and Gunn (this volume) provide recent insights from electronic tagging
studies on individual tunas and billfish in three major oceans, and in particular
some important insights about the dynamic capabilities of both Atlantic and
southern bluefin tunas in comparison to the other species that have been reported.
B. Local Weather and Global Climate Change
The presence of strongly seasonal equatorial convergence/divergence zones

and periodic Warm and Cold Events associated with the El Nifio-Southern Oscil-
lation (ENSO) impose a series of relatively frequent regional and global cause and
effect patterns in ocean fisheries (Glantz, 1992; Le Blanc and Marsac, 1999).
These patterns suggest that these and other ocean and atmospheric processes
9. TUNA OCEANOGRAPHY--AN APPLIED SCIENCE 351
stimulate or suppress regional production, depending upon where and which spe-
cies that you are interested in. There are several processes and patterns that can be
confusing, even confounding, as they differentially affect catch rates of the several
different gear types, as well as species compositions and distributions.
Monitoring both the ocean climate and the fisheries production can provide
generally useful information, while ignoring either can lead to quite misleading
conclusions about trends in both fishery resources and ocean climate. For ex-
ample, as part of these large-scale ocean dynamics, local thermocline profiles are
either enhanced or not, and the various tuna species involved may actually become
more or less vulnerable to the various fishing gears used (Sharp, 1978, 1979; Mar-
sac and Hallier, 199 1; Le Blanc and Marsac, 1999). In the case of the post- 1982 -
1983 El Niiio Warm Event, there was a dramatic decrease in vulnerability of the
yellowfin in the eastern tropical Pacific fisheries. To some analysts the changes in
catch rates signaled the long-awaited collapse of those resources, since the catch
rates had been generally in decline since the early 1970s. However, the rebound
of the thermocline following the reinitiation of the equatorial trade winds at the
end of the Warm Event led to a period of extremely high catch rates. Some advo-
cates concluded that this proved that huge resources had always existed, and that
there was no reason to manage the resources at all.
Both are, in fact, wrong interpretations. The thinning of the upper ocean habi-
tat due to the ocean’s surface heat removal, regional upwelling, and shallow ther-
moclines associated with upwelling and ocean cooling following the Warm Event
made the entire region’s tuna more vulnerable to overexploitation than at any time
in the history of the high seas seine fishery. Sharp and McLain (1993a,b) described
how the misinterpretation of conventional abundance indexes, particularly when
interpreted independently of environmental context data, is a prime cause of fish-
eries management failure.
III. PHYSICS, FISHERIES, AND

DYNAMIC PERSPECTIVES
A. Physical Structures versus Other Contextual Changes
In the western Indian Ocean, the Maldives’ tuna fisheries are the oldest docu-
mented year-round pole-and-line tuna fishery. Maldives’ 1200 islands compose
26 atolls that act as a coarse comb, filtering the impinging ocean currents to create
production features that attract pelagic fish schools of all types. For more than a
thousand years Maldivian culture had its entire economy based on the local pro-
duction of skipjack tuna, along with the production of coconut palm that provided
both food and fishing tools. Tourism is supplanting some of this economic activity,
but cannot provide food from day to day. Maldivian tuna fishermen capture reef
352 GARY D. SHARP
fishes each morning, and transfer them into the sea-water-filled hulls of their half-
submerged masdohni fishing craft, in order to portage them to the off-island fish-
ing areas. On sighting tuna schools the baitfish are chummed to attract the small
skipjack and yellowfin that are then caught using poles, lines, and barbless hooks.
For millennia, Maldivian women spent much of their days boiling, salting, and
smoking the loined fish for sale in distant markets they would never see. This
limited resource base is a rigorous test of any culture, and attests to these and all
islanders’ durability.
Several joint ventures began in the late 1970s to help modernize Maldivian
tuna operations. The traditionally sail-driven fishing fleet was systematically con-
verted to diesel engines that helped improve their ranges and mobility. Unfortu-
nately, the conversion also placed them on a petroleum economy right at a time
when tuna values were dropping and oil prices were beginning to increase. Mobile
fish collection services were initiated, where the fish were first frozen and then
transported to markets. A small cannery operation was built in 1978 with a limited
(8 tons per day) capacity. It could not provide the services needed to handle the
tuna deliverable from the many islands. A second round of value-added develop-
ment projects followed, and in 1986 a new modernized cannery was built that now
processes up to 50 tons of fish each day. While the older-styled dried and smoked
fish products continue as major market items, ongoing construction of freezer
storage facilities has increased the production of canning-quality products. These
will continue to grow, creating export products for the growing world market.
Seasonal patterns within the adjacent Arabian Sea to the north and west of the
Maldives are sufficiently dynamic and restrictive that the coastal nations and Lac-
cadive islanders to the north have only short fishing seasons (Sharp, 1995). Re-
gional fishing occurs as the more nearshore-oriented longtail tuna or skipjack and
yellowfin tuna make quick migrations through their coastal fisheries, attracted by
the wave of production induced by the onset of the southwest monsoon. Other
than the Maldives and Sri Lanka, most other Arabian Sea locations do not support
large fishery-dependent cultures because the Monsoon-induced production also
generates large areas of anoxia, precluding entry of tunas and other fishes with
high metabolic rates for many months every year. The Bay of Bengal has a much
larger oxygen-rich area and the coastal regions are only subject to local anoxia
during the peak of the southwest monsoon. Tropical tunas abound from Sri Lanka,
eastward to the Andaman Islands and Thailand, on through the shallow Straits of
Malacca separating Sumatra and Malaysia, and into the Indonesian Archipelago.
Subsistence fisheries have dominated these regions until quite recently. The more
eastern regions are unlikely to develop major tuna fisheries for export, simply due
to the historical patterns of sociopolitical conflicts and the rather disperse nature
of the resource. Tuna fisheries are evolving in this region, but there will need to
be more cooperation and organized law and order on the sea before they can
thrive.
Sharp (1992) described the relatively recent development of the high seas
9. TUNA OCEANOGRAPHY-AN APPLIED .SCIENCX 353
seine tuna fisheries of the western Indian Ocean. That development took place as
a specific result of a collation of monthly oceanographic and climate data sets over
the globe. Applying the same criteria that appeared to promote catch success in
the eastern Pacific and Atlantic oceans to the monthly mean ocean observations
in the Indian Ocean, regions of likely fishing successwere described and mapped
(Sharp, 1979). The willingness of the Food and Agriculture Organization (FAO),
Fisheries Department’s Industry Division staff, and the director of the Indian
Ocean Fisheries Development Program, Harry Windsor, to invest in the underly-
ing empirical validity of these maps was immediate. The FAO’s and Development
Program’s respective missions to promote experimental fishing resulted in the
rapid and uniquely successful collaboration between the two major high seas
resource-owning nations and foreign tuna fishing industry interests. The success
of this fishery development activity was unique and thrives today.
The Maldives and Seychelles adopted development patterns best suited to their
individual cultural legacies. The Maldives devised a locally operated national hsh-
ing project. Seychelles, on the other hand, started out by working closely with
French and Spanish fishermen-the two European nations with the most devel-
oped tuna fishing industries. After a short period of exploration and test-fishing.
the Seychelles Fishing Authority now “sells tickets,” or access rights, to its broad
Exclusive Economic Zone’s (EEZ) tuna resource base, and provides support to
visiting fleets, but does not own its own fishing vessels or markets. Both island
nations have developed into significant providers of tunas to the international mar-
ketplace, with minimal perturbations of local cultures, while their economies have
grown. To date, this region’s tropical fisheries are not in any danger of overfishing.
However, to the south and east, the fisheries for southern bluefin tuna have pro-
vided nearly 30 years of information about just why all fisheries need to be care-
fully documented, and managed, prior to the occurrence of debilitating over-
exploitation.
B. Continuous Changes in the Big Picture
The publication of the Atlas of Tropical Tuna Fisheries (Fonteneau, 1997)

culminated several years of effort to summarize all of the tuna fisheries catch
records within a single resource document, so that the evolution of these fisheries
could be traced, and patterns studied. Among the riches of these data sets are
several stories of changes in fishing technologies, marketplaces, and products, and
access to fishing grounds. Also apparent are the excesses due to the rapid expan-
sion of industrial fleets out onto the world oceans, well before management pro-
cedures or adequate information were available. Missing, unfortunately, are the
documented historical developments such as those described by Mather et al.
(1995) in the post-WWII northeast Atlantic, where tens of thousands of tons of
giant bluefin were caught each year for several years, and then nothing.
Many of the historical changes in the high seas fisheries behaviors. distri-
354 GARY D. SHARP
butions, and catch compositions reflect epochs of changes in political conven-

tion regarding ocean ownership, management, and exploitation regimes. Some
changes were due to new fishing technology. Other changes reflect the more in-
evitable, uncontrollable changes in climate-driven oceanography and subsequent
ecological responses. These latter changes occur on all time and space scales,
leaving a lot to be measured and monitored over large regions of the world’s
oceans if truly informed management decisions are to be made, and if the various
tuna populations are to be nurtured and fisheries sustained. Life-history strategies
define the patterns of environmental variations that each species has adapted to
(or not), providing insight into time and space scales over which fisheries man-
agement actions should be concerned.
The general expansion of high seas fisheries occurred in response to Cold War
politics and Law of the Sea ownership debates, ongoing long before the Second
World War. In 1976 the U.S. Congress passed the Magnuson Fisheries Conserva-
tion and Management Act (MFCMA). The Act was intended to resolve the ocean
fisheries access policies of the USA, independently from the Law of the Sea Ac-
cords. These, in turn, were being developed by a host of nations whose interests
in the oceans were motivated by recapturing the values of ocean resources from
foreign interests. The post-1976 “gold rush” onto the oceans escalated as the
MFCMA was cloned by many nations as they sought to obtain their pieces of
the action on the high seas. Within the verbiage were definitions that separated the
valuable tunas and billfishes as a unique class, the “highly migratory species”
(HMS), although many other species of fish, for example, sardine and jack mack-
erel, exhibit similar or greater migrations along shore and offshore. Surdinups
even has a similar life history, attaining maturity after 4 or so years, and living 14
or more years.
C. Changes in Markets and Resource Ownership
The special HMS category made management of these species subject to re-
gional nongovernmental management bodies rather than their being managed (i.e.,
owned) unilaterally by coastal states. Tunas and other “highly migratory species”
have thus been exploited in more than one sense in the recent expansions of na-
tional interests. Fishery interactions are debated and discussed elsewhere (FAO,
1996), and set the undertones of the aggressive nature of today’s resource owners
and would-be exploiters. As a result of the development of the Law of the Sea
Accords, and the concepts of the Exclusive Economic Zone, there emerged a new
generation of international corporations and unusually complex marketing sys-
tems. These evolve continuously in efforts to cope with changes in legal owner-
ship, access, and regional and local responsibility for resource management.
These same interests manipulate supply and demand, often creating ecological
tragedies.
For example, the southern bluefin population was severely affected by early
fishing activities, and the consequences have been enlightening, if sad. These
long-lived fishes have yet to produce any substantive year classes since the late
1960s when they were fished intensely on their spawning grounds northwest
of Australia. Long life spans, particularly of ocean species, are an adaptation to
long sequences of poor opportunities for successful recruitment (Johnson, 198 1;
Kawasaki, 1983). In their zeal to exploit the bluefin tuna resource, Japan’s fisheries
interests have evoked every available negotiation tool to continue to exploit the
clearly depleted southern bluefin stock. The issue is that this species has such an
extreme life history, with literally decades between successful year classes, that
they cannot be managed as if they were in any way an “ideal population” with an
“annual recruitment” as assumed under typical pelagic fisheries population man-
agement models. By continuing to fish down the older, principal reproductive
ages, the species is certain to undergo first economical, and then biological,
extinction.
Recognition of these limitations has yet to be assimilated into the management
of high seas resources. Well-designed ocean and population monitoring are
needed to define conditions that are conducive to both good and poor recruitment.
Le Blanc and Marsac (1999) have recently reviewed developments in environ-
mental monitoring and prediction at a broad regional scale for the Indian Ocean.
They provide a set of examples and objectives that require diverse institutions to
collaborate to provide for both more efhcient fishing operations and better overall
management. The regional collaboration between seiners and tuna management
in monitoring Indian Ocean fisheries provides good examples for other regions
(Hallier and Marsac, 199 1).
Sharp and McLain (1993a,b) also concluded that since the majority of the
world ocean is now visited more often by fishing vessels than will be covered any
time soon by oceanographic expeditions, it would be wise to encourage the fishing
vessels to participate in ocean monitoring and data sharing. This would provide
greatly needed information on a lot more than just fisheries behavior, for example,
climate change and ocean dynamics. In this light it seems that the nonnegotiable
terms of access to any of these living resources should all have built-in require-
ments that fishing vessel crews measure and report a suite of relevant environmen-
tal observations every day they are at sea. The data should be treated and distrib-
uted as part of the global weather observation reporting system. This way, ocean
measuring and monitoring systems in the ocean can finally be brought into a state
of utility such that none of the usual climate, oceanography, and fisheries issues
needs to be debated-due to the usual absence of information.
Fish behave from minute to minute, hour to hour, and day to day in response
to oceanographic, atmospheric, and solar-lunar processes that operate on similar
time and local space scales (ICANE, 1981; Kendall et al., 1996). Also, the daily
development of ocean features has been among the recent several decades’ lessons
356 GARY D. SHARP
from both in situ and high-resolution satellite-mediated studies of ocean climate

and weather-related phenomena. However, and despite agency rhetoric, the weak-
nesses of satellite irradiance sensor data (Clancy and Weller, 1992; Sharp, 2000)
are such that most of the world’s productive fishery regions cannot be well moni-
tored at operational time and space scales from irradiance sensor-based platforms
during the most productive periods, except in a very cursory sense. The problem
lies in the interactions between atmosphere, clouds, marine layer moisture, and
productive ocean processes that promote fisheries. The best fishing conditions
tend to blind satellites to the ocean’s processes, and even more limiting, satellite
sensors cannot measure subsurface ocean processes.
The seasonal expectation from any location is defined as climate, while what
actually happens is defined as weather. Similarly, the ocean weather that matters
to individual fishes occurs on time and space scales that defy monthly or longer
temporal aggregations for use in more than cursory summaries of cause and effect.
Fishing effort, on the other hand, is more often than not monitored through indus-
try, national, or regional fisheries management bodies. However, individual fish-
ing vessel locations and catch statistics are typically unavailable to any but agency
staff, as a condition of their being made available to the managers. Another con-
founding consequence is related to casual use of temporal aggregations. Choice
of an appropriate seasonal calendar is more of an issue than one might assume,
given that the ocean is dynamic on all time and space scales. In order to understand
both short- and long-term responses, research and data analysis need to be based
on synoptic measures of fish behavior, environmental status, and trends. These
often reflect local to regional scale processes, but are not tied to specific Julian
calendar dates. In this sense, the separation of catch and effort data sets into either
quarterly or multiyear epochs for the entire globe can be quite misleading.
Oceanographers have come to understand that for each region there are unique
symptoms of seasonal processes. Expectations change as a function of changes in
climate-driven ocean states. Upper-ocean temperature profiles, salinity, and pro-
ductivity are all more or less bounded within annual seasonal cycles as functions
of insolation, wind speed and direction, and freshwater inflows. For example, each
locale has climatological or mean dates for peak surface warming; maximum
northern or southern extent of ocean surface warming; or cooling that is a result
of upwelling or onset of surface heat-scouring winds. In the Indian Ocean the
dominance of the seasonal monsoons has provided the needed navigational secu-
rity of seafarers for millennia, as the winds reversed on a fairly consistent sched-
ule. They could “ride the wind” from one point to another in one season, and
return with the next. The northeast monsoon blows from Asia’s plains into the
southwest Indian Ocean from December to April. The southwest monsoon blows
in the opposite direction from the Indian Ocean into Asia’s highlands, starting in
about June and continuing until October of most years. Yet there are systematic
trends that shift these onset dates in both space and time (Sharp, 1995).
The ENS0 Warm/Cold Event fugue is the most frequent perturbation of “ex-
9. TUNA OCEANOGRAPHY--AN APPLIED SCIENCt 357
petted” seasonal ocean patterns. Understanding them enough to make credible

forecasts has been elusive (Enfield, 1989; Barnston et al., 1999). El Nifio Warm
Events, or La Nifia Cold Events, are the anomalous years. El Nifio years can cause
severe drought across the Asia-Southeast Asia region, and La Nifia episodes can
cause flooding, and downstream eutrophication and increased ocean production.
There are also longer trends within which the ENS0 climate perturbations are
superimposed. Fisheries resource bases shift along with them, as measured by
changes in catches, distributions, and species composition. This information is all
well documented in the recent climate debates, as well as in fisheries literature
(Sharp and Csirke, 1983; Glantz and Feingold, 1990; Marsac and Hallier, 1991;
Sharp and McLain, 1993b; Beamish, 1995; Gauldie and Sharp, 1995; Glantz,
1996; Lehodey et al., 1997; Klyashtorin, 1998; Le Blanc and Marsac, 1999).
There are also long, slow patterns of changes in the onset dates, as well as changes
in mean wind speeds, and ocean consequences, over time.
Short-term perturbations such as ENS0 events promote long-lasting physical
responses and ecological responses. Here is a situation where one can attest to the
utility of satellite remote-sensing tools, where high-resolution radar is used to de-
termine sea level height (SLH) changes on the order of meters. In the tropics, in
particular where sea surface temperatures (SSTs) may not be dynamic, these SLH
changes are direct indicators of thinning (thickening) of the upper mixed layer.
and hence enhanced (lessened) vulnerabilities of the tunas to specific fishing
methods and gear. As pointed out previously, regional tuna catch characteristics
are good indicators of ENS0 phases. To put all this in perspective, the 20th cen-
tury has had the lowest frequency (28) of Warm Events since the 17th century
(29), which was the coldest period within the recent five centuries. The 18th and
19th centuries experienced 47 and 49 Warm Events, respectively, suggesting that
the baseline of event frequencies (expected recurrence interval) changes signifi-
cantly on decadal to centennial time scales. Ecological patterns shift with these
processes within regional ocean ecosystems.
Only recently have the noncoastal, open ocean phenomena that affect the life
histories and behaviors of the large migratory species come into focus. They had
not been as well defined previously. Suzuki (1989), for example, posits that most
of the world’s tuna fisheries’ recruitment benefited from the 1982-1983 Warm
Event. Marsac and Hallier ( 199 1) showed that the I 990 - 199 1 decreasing trend in
catch rate for the western Indian Ocean seine fishery was related to the thermo-
cline deepening associated with the 1990 - 199 1 ENS0 Warm Event. They, fortu-
nately, had a rich data time series, including the oceanographic observations, from
which to formulate their explanation and test its validity. After introduction of
these concepts in the early 198Os, one of the criteria for access set by the Sey-
chelles Fishing Authority was the requirement for an onboard observer program
to collect standard oceanographic observations, as well as mandatory logbooks in
which fishing operation information was to be kept. In their review of Indian
Ocean fisheries and climate processes, Le Blanc and Marsac (1999) identified
358 GARY D. SHARP
many aspects of the seasonal, decadal, and epochal climate-driven ocean proper-
ties that affect tuna fishing. They also provide examples of high and low SO1
phase-related surface dynamics for the Indo-Pacific regions affected by the ENS0
cycle on seasonal, annual, decadal, and centennial time scales.
Fisheries and fish population responses can be easily misinterpreted. Good
ocean observations are necessary to go along with several years of age-distribution
and recruitment data from which to track and interpret these events in order to
corroborate interpretations. It can also be entirely misleading to aggregate fisher-
ies catch data sets without regard for regional and ocean basin climate-related
processes, or by using strict Julian calendar quarters. One of the most informative
fisheries environmental presentations that I have ever witnessed was a weekly
sequenced display (by Francis Marsac) of the tuna seine fleet’s catch records
mapped over the western Indian Ocean, for the early decade of its operations. The
evolution from the seasonal upwelling along the southwest coast of Madagascar,
northward and seaward as the monsoon-driven ocean features progressed from
year to year, proved that my 1979 insights were correct. The interannual variation
was also notable, and important.
IV. A BRIEF REVIEW OF HIGH SEAS TUNA

FISHERIES DEVELOPMENT PATTERNS
Fonteneau (1997) collated available catch records, and charted historical pat-
terns, by fishing gear type. Among the most valuable contributions of the Fonte-
neau Atlas is in providing a visual record of the major changes in effort and catch
patterns since the mid-1950s. Three distinct fisheries histories were created by
separation of the information into pole-and-line, seine, and longline gear types for
the decadal epochs 1956-1968,1969-1978,1979-1988, and 1989-1993. Many
regional fisheries have been in production for several hundreds of years before
these Atlas summary periods. For example, the previously described Maldivian
skipjack fishery was well developed and strong long before these Atlas records
start, as were the Japanese home island and longline fisheries of the western Pa-
cific Ocean. The eastern Pacific, Bay of Biscay, and Azorean coastal tuna fisheries
were also well developed, and the Mediterranean trap and harpoon fisheries were
ancient (Mather et al., 1995; Bard and Santiago, 1998).
A. Innovations in Technology Play Major Roles

in Recent Changes
Examination of the initial catch levels recorded in the 1956-1968 Atlas maps
through to the more recent epoch shows that all these old fisheries underwent
changes. Many declined or ceased operation, while others grew. Most of these
older fisheries were transformed from already productive old technologies into
more modernized fisheries supported by cold storage and delivering fresh-frozen
export products. For example, today most Indian Ocean tropical tuna catches are
primarily processed by Thailand’s thriving canning industry, started up in the early
1980s. Many traditional fisheries underwent similar transformations.
New fisheries have been initiated over large portions of the world ocean. An
important innovation was the general implementation of the fish aggregation de-
vice, or FAD technology, that helped many tropical fishermen to become more
efficient. Fish aggregating devices (FADS) were studied in the late 1970s and
1980s off Hawaii, as well as in the tropical Pacific surface fisheries, as scientists
sought resolution to efficient fish school location-and then bycatch issues that
will be discussed later. Some were amazing success stories. For example, the Phil-
ippine island coastal tuna fisheries developed and grew, based on their use of pi-
yaos, or tethered bamboo fishing platforms (another form of a FAD). From and
around these piyaos immense amounts of small skipjack and yellowfin (and very
large adult yellowfin) have been fished, using handlines, hook and line, and long-
lines. More recently, from the profits of these less technological fishing activities.
Southeast Asian corporations have invested in modem high seas purse seines,
creating “boomtowns” such as General Santos City in the southern Philippines, a
major industrial center built to support these new fisheries. A systematic look at
these developments tells several informative stories.
B. Pole-and-Line Baitboats
Skipjack tuna dominates the pole-and-line fisheries of the world, although

each of the other species is caught, in some seasons, within their normal annual
migrations or for particular local markets. Most of these fisheries, as plied in the
tropical oceans, were initiaIly set up as day-fisheries, leaving the dock after ob-
taining baitfish and fishing nearshore for various seasonally productive locations.
These include the small coastal fisheries operating from Baja California south to
Northern Peru, and the Atlantic fisheries based in the Azores, Madeira, the Bay of
Biscay, and Cape Verde, and along the coasts of west and equatorial Africa, as far
south as Ghana. Sri Lanka, Thailand, Malaysia, the Andaman Islands, and Indo-
nesia have poorly documented day-fisheries for tunas. Papua New Guinea’s joint-
venture pole-and-line fishery came, and went. All these fisheries experience dis-
tinct seasonality, a symptom of migratory behavior by these fishes in response to
regional climate-driven oceanography.
In the Pacific, the Hawaiian Islands tuna fisheries were created by late 19th
and early 20th century immigrants from Okinawa and other Asian fishing centers
to service the local island community’s fresh fish needs. In the 1950s Honolulu
became the location of a Bumble Bee tuna cannery that processed the local fresh
(unfrozen) skipjack into one of the best canned tuna products ever produced. Their
360 GARY D. SHARP
operations were subject to seasonal production limits and longer-term trends in

fishery production. The cannery was operated at the whim of the seasonal ocean
currents.
On the other hand, some pole-and-line fisheries were more versatile, and de-
veloped long-range tactics early on. For example, the California-based baitboat
fishery operating along the Baja California coast from the 1930s to the 1970s
fished on small (40-65 cm) so-called school fish, using chipped ice at first, and
then ammonia refrigeration and circulated brine, to conserve them. In some years
these would be mostly skipjack. In others, as much as half the catch would be
yellowfin. After WWII Asian fresh fish markets in Los Angeles began offering
premium prices for larger, fatter tunas. These included the summer run Pacific
bluefin that routinely migrated up from the local banks off the southern Baja Cal-
ifornia peninsula, along shore northward to Isla Guadalupe, and onward into the
Southern California Bight.
Throughout the 1950s and into the mid-1960s it was also common for the
baitboat skippers to make a circuit from the coastal “local” banks offshore to San
Benedict0 for an afternoon of two- and three-pole fishing for large yellowfin and
occasional heavy bigeye for these markets. They would often continue their off-
shore run by sailing westward overnight to the Revilla Gigedo Islands, to Rota
Partida, and onward to “Cadillac” or “Brito” bank, and then head northward back
to Isla Guadalupe to top off with some fresh bluefin, or back to the bait grounds
along the coast. The larger specimens would reach weights of several hundred
pounds, and careful handling brought good prices.
There was a post-WWII development in southern California of long-range
baitboats. The larger “tuna clipper” fishery from San Diego would sail due south
from Cabo San Lucas, if they had a load of good bait, to Clipperton Island. Once
they had tried their luck, or run out of bait, they would then either head due east
for Costa Rica, or sail east-southeast onward to the Galapagos Islands and asso-
ciated banks. There they would be able to find abundant baitfish, and also large
yellowfin and bigeye tuna with which they could more quickly fill their holds.
These vessels and crews were true explorers from old European stock. A good bit
of offshore exploration, using sounders and sharp-eyed lookouts, led to an ever-
broader distribution of fishing activity.
Baitfish was this fishery’s limiting resource. The typical cyclic pulsing of sar-
dine and anchovy populations caused these more exploratory fishermen no end of
grief, as each region’s baitfish would flourish, and then disappear for a season or
longer. Expansion southward eventually induced several joint ventures with Cen-
tral and South American industries, where today several landing sites and canner-
ies serve local baitboat fleets and foreign-flagged superseiners buying and pro-
cessing their catches nearer the fishing grounds.
Meanwhile, in the mid-1960s, the California fleet moved southward, and off-
shore, as the Okinawa-styled Japanese home island fisheries that were operated all
around Japan for several centuries also began expanding southward. They moved
offshore and well into the southwest Pacific Island fishing grounds, creating new
fishing communities. Local competition grew as fisheries development programs
were promoted by either the UN or the Japanese Aid agency (JICA). Hawaii’s
only cannery closed in the late 1970s. The local skipjack fishery was reduced to
focus on only local fresh fish markets. By the early 1980s many of the Pacific
Island communities either formed their own fishing fleets or made contracts with
Japanese and U.S. firms to expand their local fishing activities. Soon thereafter,
their pole-and-line catches were diluted by the expanding tuna seine fleets that had
quickly evolved from the sturdy southern California tuna clippers.
Similarly, west equatorial Africa’s baitboat fisheries evolved, as described be-
fore, from Portuguese traditional fishing styles and through Japanese fisheries de-
velopment projects. Fishermen from Cape Verde also emigrated to Brazil in the
late 1970s and early 1980s. Brazil’s pole-and-line fishery developed in the late
1970s and operated by taking advantage of the local Surdinellu for bait and nu-
merous oil platforms (that act as FADS) near Cabo Frio, where strong upwelling
attracts tropical tunas. These were all short-range fisheries, and many were day-
fisheries.
C. Purse Seines
One of the great innovations in tuna fishing took place in the late 195Os-
Marco Puretic’s hydraulic “power block,” designed to handle the new seine nets
that had been scaled up from sardine seines to meet the demands of high seastuna
fishing, particularly for large-volume skipjack and yellowfin schools. There were
numerous styles of fishing and different approaches to each type of tuna, depend-
ing upon the boat owner/operator’s objectives. Some of the older low-deck
wooden California sardine and salmon vessels were readily converted to heavier
tuna seine gear. Individual skippers specialized in seasonal runs to the bluefin
grounds, where they would fish only at night for the coveted large-sized bluefin,
rather than scramble for skipjack schools among the throngs of baitboats.
Night fishing is an art, and requires a lot of coordination. The tuna vessels
were operated without any visible light, except for a single powerful flashlight in
the crow’s nest that was swept about periodically to mark each vessel’s location in
areas where more than one boat was working. The nets were set around “glowing”
surface schools, as the fish school’s passage caused the plankton to fluoresce.
Some of these vessels and crews got very proficient, and were able to fill their
holds, unload, and be back on the grounds, often several times, before similar-
sized baitboats working the “school fish” from dawn to dusk made a full load.
One early lesson was that bluefin tunas passed their nights near the ocean surface.
As the California fleet began to age, or shift from wood to steel hulls, the new
vessels were outfitted with seine winches and power blocks, and sailed offshore
362 GARY D. SHARP
and away from the coastal baitboat action. Many families made their fortunes just
after the Second World War by investing in these new wider-ranging boats. The
tuna purse seine fishermen had already made the switch from coastal day-sailors
and nearshore fishermen to the high seas. They designed and built larger new
vessels that were self-contained, seaworthy, and livable, as the timethat they spent
on the ocean was extended in order to fill these big, expensive-to-operate vessels.
They delivered premium fish in large loads to ever more capacious canneries.
The tuna clipper and seiner skippers soon discovered that skipjack and small
yellowfin would aggregate about floating objects, for example, logs, dead whales,
and even their own fishing boats while they were shut down and adrift at night.
They began marking logs (or various portable FADS) with radar reflectors or
lights, in order to track them all night. By early morning’s first light these fisher-
men could be ready to set their nets around these natural (or artificial) FADS, and
haul in a good size catch before setting off to find surface schools for the rest of
the day. There were often several other nontuna species (e.g., dolphinfish, turtles,
sharks, rainbow runners, and assorted small fishes) associated with the FADS that
were captured in the nets, sorted, and returned to the sea, or eaten by the crew.
Beyond this general shift in efficiency, the fishermen discovered that larger yel-
lowfin tuna-more valuable than the smaller schooling skipjack, yellowfin, or
bigeye-were attracted to and also schooled beneath “porpoise” or dolphin
herds. In 1967, the Inter-American Tropical Tuna Commission (IATTC) began
officially “managing” the eastern tropical Pacific yellowfin fishery within a well-
defined Commission Yellowfin Regulatory Area (CYRA). The vessels could fish
outside the CYRA once catch quotas were attained. Another kind of race was on.
Starting with yellowfin fishery regulation in 1970, the California seine fleet
would spread westward after the closure of the CYRA to fish on dolphin-tuna
aggregations. By this time, new larger, faster steel seiners were emergent, stimu-
lated by loopholes and mandates in the IATTC regulations. Marco Industries
thrived as they scaled their power block and net handling gear to ever larger ves-
sels. The high seas seine fleet was now focused on dolphin herds rather than
schoolfish aggregations. Also, the idea that yellowfin reproduced mostly around
coastal islands was soon dispelled. Full age structures were located out on the high
seas. Unique cohorts were found at some locations, appearing only in seasonal
situations as they followed seasonal oceanographic features. Yellowfin fisheries
from Baja California south to Central America had two 6-month cohorts; in the
southern coast region, one slightly off-cycle cohort dominated (Sharp, 1978).
These were often “joined” by unique cohorts from offshore sources.
The vessels were able to increase their production from yellowfin as a “by-
catch” in their dolphin fishing ventures in the offshore regime. The fishermen
discovered that the dolphin herds quickly learned to avoid their vessels, so they
created a new type of fishing crew member, the “speed boat” or chase boat driv-
ers, whose job it was to herd the dolphins into position so that the ever-faster
seiners could set their ever-larger seine nets around them so as to catch the asso-
ciated yellowfin tuna. Some of the smarter, or perhaps only more desperate, dol-
phin herds responded by learning to break up into smaller herds, in a “starburst”
behavior, as they heard the seiners coming over the horizon. Now the skippers
bought faster speed boats, and more of them. Some skippers with their newer
bigger boats hired helicopters, pilots, and “chopper mechanics” in order to locate
ever more elusive dolphin herds. This became one of the most costly fishing meth-
ods ever devised.
These earlier efforts resulted in longer, faster, more stressing chases that some-
times caused situations where many hundreds of dolphins might be killed during
a set of the net, affecting the time needed to remove the tunas from the net, and
causing no end of handling problems. This was not an easy situation for the fish-
ermen, either, as they were now also forced to deal with the dead weight of these
large mammals, as well as the usual fish handling routine. They, too, responded
quickly by working on methods to minimize the numbers of dolphins retained in
the net before the net haul was finalized. Installation of “Medina panels” in the
seine nets and perfection of the “backdown” procedure were well deployed within
the U.S. fleet by the mid-1970s.
The Bumble Bee cannery in Honolulu began processing some amounts of the
offshore catches delivered by the high seas seine fishery. However, they were not
set up to handle large production and vessels would be tied up for extended pe-
riods waiting to unload. Eventually, the public outcry regarding dolphin deaths
that forced the fishermen into a legal compliance situation collided with the eco-
nomics of the oil crisis of the early 1970s and the increasing economic competi-
tion due to a general overcapitalization. As a result, many of the US. vessels were
sold, and others went even further offshore, into the west and south Pacific, where
dolphins and competition were not an issue. As the situation evolved, many of the
U.S. vessels moved even farther south and west, making Hawaii a less attractive
delivery point.
However, access to the numerous Pacific Island economic zones needed to be
negotiated. As well, the issues of delivering catches from distant sources needed
to be addressed. The capacity of the small cannery in American Samoa was in-
creased to handle the larger loads delivered by these giant superseiners, a system
of trans-shipping ports was created to handle these larger vessels’ catches, and
other canneries were planned around the Pacific Island community and Indonesia.
The effects of these developments are important to understanding the patterns of
the expansion of the seine catch and effort statistics, and eventual concentration
of particular seine and baitboat operations near the regional processing plants.
Meanwhile, in the mid to late 1970s the Spanish and French were undergoing
similar growing pains. Their tropical Atlantic seine fleets expanded well offshore,
away from the traditional baitboat fishing grounds. Catch rates quickly rose, and
then began to decline. Competition due to overcapitalization was cutting into their
economic viability. This was resolved in an unusual, but reasonably positive way.
In the early 1980s the FAO efforts to develop the Indian Ocean tuna fisheries
364 GARY D. SHARP
had been initiated. Both Spanish and French tuna industries were working toward
gathering information about the availability of tunas around and about the western
Indian Ocean. Several Spanish baitboats were sent to test-fish in and about the
Seychelles Islands and over the Plateau-they understood that superseiners were
unable to work there due to the working depth of their large nets. Although they
could catch reasonable amounts of fish, there was no place for these small bait-
boats to unload their catches. It also cost nearly half their market value to trans-
ship them to the nearest processing ports in the Atlantic or western Pacific oceans.
The larger seiners, however, could catch larger quantities, from a larger resource,
and ferry their catches to distant ports for unloading and remain profitable. While
the seine operations proved economically feasible, the baitboat operations were
abandoned. Meanwhile, the Seychellois developed their strategy for pricing ac-
cess to their EEZ and its tuna resources. The catch processing problem was soon
resolved by Thailand when they decided to open a tuna processing facility for
Indian Ocean and western Pacific tuna. They now dominate world canned tuna
exports.
So, with a little historical perspective, we can explain much of the evolution
of the surface fishing effort as outlined in the Fonteneau AtEus. However, the most
interesting patterns over this period are those of the longline catch and effort. They
display a combination of operational decisions, investments, changing market
strategies, and fishery-induced and oceanographically driven population shifts
over the period from 1956 to present.
D. Longline Fishing Pattern Changes
The early (1956 -1968) records of catch and effort distributions from the long-
line fleets show widely distributed, primarily Japanese owned and operated high
seas operations that were focused on Pacific and Atlantic ocean albacore, yellow-
fin, and bigeye; eastern Indian Ocean southern bluefin; and northwestern Pacific
swordfish. The significant shifts during the 1970s were signaled by more broadly
distributed and higher catches of bigeye and less albacore in the North Pacific,
indicating that the gear had been extended to fish deeper to target the more valued
bigeye. This, of course, was the result of direct industrial applications of Japanese
vertical longline research referenced above and behavioral studies done in the
mid-1970s by Hanamoto (1974, 1975). During the 1979-1988 period catches in-
creased and the broadening fishing effort was, again, tightened up and focused on
large bigeye, albacore, and large yellowfin in their respective habitats (Hanamoto,
1987; Uosaki and Bayliff, 1999).
The newly emerged shallow longline fishery for yellowfin in the northern Ara-
bian Sea was unique. It was focused on tunas that are most likely trapped within
this warm region. They are constrained from entering the deep water habitat by
the high-salinity, low-oxygen water from the Gulf environment as it spills over the
sill at the Strait of Hormuz, into the Oman Gulf. Once into the Arabian Sea, this
low-O, watermass sinks and spreads out at middepths across the seasonally oxy-
gen-deplete Arabian Sea, and southward into the subequatorial Indian Ocean. This
low-oxygen water in the Arabian Sea locks those predators with high metabolisms
into a constrained surface habitat along the coasts of northern Oman, eastern Iran,
and western Pakistan.
After the early ( 1956 -1968) decade there was also a significant shift from the
highly exploited eastern Indian Ocean southern bluefin spawning ground fishery
in the third and fourth quarters to the more southerly focus of the south of Austra-
lia, New Zealand, and South Africa. Although this effort pattern persisted, catches
declined in the 1980s and early 1990 records, suggesting that the resource was
heavily overfished, and has yet to recover. The continuing escalation of interna-
tional conflicts over Japanese demands on this resource will continue to cause
conservation-minded citizens no end of anguish until the situation is resolved.
From the records, the Southern Ocean longline effort that was once aimed at
southern bluefin seems to have been retargeted slightly to the north, into more
transitional waters, for albacore.
The Atlantic bluefin longline catches in the North Atlantic and Mediterranean
appear to have evolved from two early minor fisheries, one that remains intact and
progresses from fourth quarter activities on the Grand Banks to the warmer up-
welling area south of Cape Hatteras in the following (first) quarter, and another
that occurred off northeastern Brazil before 1968. As was explained to me by the
late Luis Rivas (Rivas, 1978), this latter bluefin catch was primarily made by a
Cuban fishery operating on mature bluefin that aggregated during the second quar-
ter on a massive seasonal squid resource. When the squid no longer appeared, the
target bluefin disappeared from the region, long before any management was im-
posed. No one has any clue why the squid disappeared, as they were not heavily
exploited by anyone. Whether the bluefin tuna no longer aggregated off north-
eastern Brazil due to their food supply disappearing or due to being fished is
unresolved.
The patterns of longline swordfish catches also changed dramatically from the
early period into the present decade. The catches that were once limited to a near-
bycatch fishery in the Pacific Ocean albacore and bigeye fishery east of Japan
shifted over two decades to the seasonally dynamic tropical Atlantic activity
dominated by Japanese and Cuban vessels. Additional new swordfish longline
fisheries grew over the period, one off Argentina and others off the eastern USA
and Canada into the Gulf of Mexico and the Caribbean. This latter longline sword-
fish fleet grew rapidly, and was clearly overexploiting the resource in the early
1980s. The fleet dissipated as many of the southeastern fishermen moved their
vessels to Hawaii to begin development of a new Hawaii-based longline fishery
for swordfish and bigeye tuna. The remaining longline effort comprises smaller,
seasonal longlining activities that target yellowfin in the growing fresh tuna (ahi)
366 GARY D. SHARP
markets along the eastern seaboard and Gulf of Mexico. Although not a true by-
catch, the swordfishery has shown constant signs of decline and debility since the
late 1970s despite the vessel departures. This may have as much or more to do
with longline effort outside the EEZ than with coastal fisheries.
E. Ongoing Changes in Longline Fleets

and Fisheries Interactions
Significantly, the recent trend in tuna fisheries research is in studies of fisheries

interactions, as reviewed by Shomura et al. (1994, 1996). Boggs’ (1996) discus-
sion of “Unresolved Problems and Questions from the [ 19941 FAO Consultation
on Interactions of Pacific Tuna Fisheries” centered on the major contributions
from tag and recapture studies in the history of tuna research in support of man-
agement. While no one would disagree that basic operational fisheries information
and biological sampling from the catches provide the most important information,
the interpretation of these data needs to be carefully moderated from synoptic
contextual information (Sharp, 1987). The common fallacy has been to treat the
variations in catch as due to population responses within environmentally induced
“noise.” The facts are that fisheries are first and foremost direct consequences of
their changing environmental contexts, and as such, cannot be treated as if they
were (1) somehow subject to either “inherent stochasticities,” or (2) stable, unless
otherwise determined.
Bertignac and Ardill (1996) provide useful insights into the recent develop-
ments in the Indian Ocean tuna fisheries-from the rise of the western Indian
Ocean high seas seine fishery, to the short-lived rise and fall of industrial drift
gillnetting for albacore. The most significant recent development has been that of
the entry into the eastern Indian Ocean and Arabian Sea of “hundreds of long-
liners (mainly under Taiwanese and, more recently, under Chinese registry).” Ex-
cept for a few joint ventures and charters, Indonesia has the only other substantial
domestic longline fleet operating in the Indian Ocean. Although these fleets target
mostly yellowfin tuna, south of Java southern bluefin are also targeted. Catch re-
ports and biological sampling are rare.
Bertignac and Fonteneau (1996) describe similar interactions for the western
Pacific fisheries. These new fleets are spreading out along the coasts, and then
offshore, to fish on the same, or mixtures of, adjacent resource bases that supply
the cultural nearshore fisheries. Conflicts are inevitable, and both sociological and
ecological consequences of the spreading of fishing effort will vary, depending
upon location and historical patterns. The management problems are associated
with invoking responsible vessel ownership, monitoring multinational corporate
management, and the tractability of obtaining useful data from such fleets. None
of these are trivial issues.
A similar transition that needs to be watched is the refitting of Gulf of Mexico
shrimp trawlers with longline gear, and their movement into the Pacific swordfish
and bigeye fishery offshore of northern South America. In the eastern Pacific re-
gion just south of the equator, longline fisheries regularly land more prime sa-
shimi-quality (high fat content) bigeye than are found anywhere else in the Pacific
Ocean. The issue there is that the Japanese, in their long-term plans, made large
investments in newly designed high-tech vessels with onboard blast-freezing
equipment that were focused on the bigeye fishery south and west of the Galapa-
gos Islands, extending offshore and southward into the Marquesas Islands. In the
recent decade there has been a convergence or superimposing of several develop-
ing purse seine fleets in the Pacific region. The seiner fleets depend upon fish
aggregating devices to attract the region’s abundant skipjack schools. Unfortu-
nately, these schools are often observed to have mixed-in undersized (<40 cm)
yellowfin and bigeye that are discarded since they have low market value. This
bycatch, although not great in weight, turns out to be huge in terms of numbers of
individuals. The result has been severe declines in the recruitment of bigeye into
the longline fishery, which depends upon fish of greater size and age for its eco-
nomic success.
Hall (1996, 1998) has described the evolution of the tuna-dolphin problem
and the likely ecological impacts of this regional situation that was caused by a
shift in fishing technology to accommodate the need to minimize exploitation of
dolphins in tuna fishing operations. These enlightened perspectives have begun to
swing the pendulum of public, international, and agency opinion back toward sup-
port for careful, more rational fishing on dolphin-associated yellowfin schools.
using simple, valid ecosystem arguments, and recognizing that dolphin death rates
can be controlled.
F. Ocean Climate Changes and Fishery Responses
ENS0 Warm Events cause a general spreading of the Warm Pool east and west
(Forsberg, 1980; Lehodey et al., 1997, 1998). Thus, more of the smaller, Warm-
Pool-associated skipjack spill over into the eastern half of the Pacific Ocean to
compete with their larger, cool-ocean-adapted cousins, as well as westward into
the Indian Ocean. In contrast, the release of the ENS0 Kelvin Wave from the
Warm Pool allows the habitat of the three large tuna species living at depth in the
western Pacific Warm Pool to emerge. This phenomenon, in turn, makes these
larger tunas more accessible to both surface fishing gear and longline fisheries.
Not unexpectedly, the availability of surface schools of skipjack in the described
region has been observed to be greatest since the onset of the recent decade or so
of increased ENS0 Warm Events. A general warming trend occurred along this
equatorial eastern Pacific region that is usually described as being dominated by
influences of the Humboldt Current’s colder upwelled water and trade winds. The
westward trades tend to scour away surface heat, and cause the thermal profiles to
368 GARY D. SHARP
be steeper, and surface temperatures to be cooler, in general. With an enhanced

warmer surface layer, skipjack and yellowfin from adjacent north, south, and
west habitats have converged, creating a concentration that, in turn, has attracted
seiners.
One might wonder whether the patterns of ENS0 observations that indicate a
several-decade-long upward trend in frequency of Warm Events might continue,
and reinforce the growth of the affected region’s surface fisheries, causing further
declines in longline catch rates for bigeye tuna. This could cause further economic
erosion of the longline fishery. If, on the other hand, the trend were to slow, re-
verse, and return the region to cooler SSTs and shallower thermoclines, the growth
of the surface fishery might be suppressed, or reversed, and allow a few more
recruits to the longline fishery for older, larger bigeye. Of course, an alternative
scenario is that a cooler period might simply spread the surface fishery north and
south, and along with the shallow thermocline, make these regional fish even more
vulnerable, resulting in an increase in this fishery’s debilitating effects over an
even larger area. The point here is that dynamics in these fisheries reflect climate
variations.
These are important questions and suggest one of the purposes of gathering
and using time series of climate and ocean observations, along with closely asso-
ciated fisheries data. Even rich fishery data sets are not really very useful without
good empirical environmental information. The oceanographic and climate data
provide context or bases for believing that certain conditions or changes in con-
ditions will affect the resource’s availability and vulnerability to the various fish-
ing methods and gear types. Along the way we have learned that there are obvious
generalities evident from comparisons of the patterns of surface and subsurface
fisheries within a well-measured ocean regime. What is good for one is rarely
good for the other. Increased catches of larger tuna are an early biological signa-
ture of ENS0 Warm Events in the western Pacific Ocean, while, as we have dis-
cussed, schools of smaller Warm Pool skipjack spread westward. The physical
dynamics and ecological responses promote the success of tuna reproduction, too.
Enhanced post-Warm Event recruitment in tunas is well recognized, although dif-
ficult to discern from simple changes in availability.
In recent modeling exercises, Lehodey et al. (1998) explore forecasting ocean
production centers and tuna forage as a means for predicting local availabilities
and abundances of these widely dispersed and highly mobile species. Referencing
the basic studies by Okubo (1980) of the behavior of small planktonic organisms
within a dynamic physical and biological oceanographic milieu that dominates
their short-term distributions and evolved behaviors, Lehodey et al. (1998) show
that over the ocean basin scale, their estimations of concentrations of food species
follow a generic pattern that includes the highest densities of high catches in the
Warm-Pool-related fishery. That is a reasonable expectation. This is a very useful
example of the integration and application of many subdisciplines throughout the

ocean sciences and ocean modeling communities.
On the other hand, Bertignac et al. (1998), in a companion paper, suggest that
there is an analogy between the random and directed skipjack tuna movements
and the diffusion-advection paradigm (Okubo, 1980; Sibert and Fournier, 1994)
in the creation of a simulation-a so-called spatial population dynamics model.
The objectives were to examine the distributions of fish concentration centers
and then, using satellite color sensor data and seasonal SST climatologies, to fore-
cast the most productive fishing areas, using an underlying population dynamics
model. What seems obvious from a historical perspective is that the results for the
more antitropical and eastern Pacific regions fit the early Barkley et al. (1978)
paradigm for the ecophysiological type of skipjack tuna for which they had esti-
mates, but their population model is based on a Warm Pool physiological type.
Such modeling activities only marginally reflect the distinguishing factors be-
tween the two recognized patterns of growth and maturity patterns (Sharp, 1978).
While I would not argue that their simulation with an L-infinity in the mid-60 cm
does not represent Warm Pool skipjack, it would be inappropriate as a simulation
of either eastern tropical Pacific or Polynesian skipjack, where immature fish are
found at much larger sizes, and adults can attain 90 cm or more.
Sibert et nZ.‘s (1999) application of the advection-diffusion models for tuna
movements, using minimal tag and release data, continues to be mired in assump-
tions. Using the entire available SPC tagging data set, there is no explanation of
the tag return function relating time-at-large and distance traveled. These func-
tions have a general shape in most tuna tagging studies. For example, in the
eastern Pacific Ocean, yellowfin tuna tagging has been active for over 40 years.
Most (>99%) of the several tens of thousands of returns were recaptured within
1200 nautical miles of their release, with up to 50% or so of those returns being
within a month or so and within a hundred or so miles from the release sites. The
distribution of the return distances have depended entirely on tagging locations
and local properties (islands, banks, seasonal ocean convergences, etc.) relative to
adjacent aggregation areas. A similar relationship is obvious in a figure (Figure 5,
p. 392, Sibert et al., 1999) where 20 of the 40 or so well-matched or best predic-
tions among the several hundred made are found within the three primary regions
of maximum tagging activity and intense local fishing effort.
By employing the short-term tag returns, Sibert ef aZ.‘s analyses of the models’
efficacies are seriously biased, as discussed by Gauldie and Sharp (1995). Gauldie
and Sharp matched the monthly ocean climatology of the 30- and 90-m tempera-
ture distributions to the patterns of the observed skipjack tuna movements to the
same data sets that Sibert er al. (1995) employed. We showed that there were
strong seasonal north-south movement patterns, and predicted similar east-west
patterns, associated with ENS0 dynamics. Lehodey et al. (1997, 1998) confirmed
370 GARY D. SHARP
that prediction. We also found less than 100 of the several thousand SPC tag re-
turns to be useful in long-term, distance-traveled estimations. The point to make
is that there is little predictive value for those tags not caught beyond their imme-
diate release areas, or within a relatively small distance from one fisheries activity
center and adjacent aggregation locations. This was known from previous studies,
and recent efforts continue to confirm this. The remaining small numbers of tags
captured long distances from their tag and release locations provide only hints
at outer bounds of the ranges of these fishes. Due to the limited development
of high seas fisheries for skipjack during the intense tagging period, the returns
mostly represent the localized distribution of regional fisheries more than gener-
alizable tuna movements. Typically, the few extreme tagged fish movements are
usually plotted up as arrows in managements’ annual reports, in order to assume
ever-larger regional resources. Why more fish do not join the ranks of these wide-
ranging individuals is likely explained best by the “leakage” from homing popu-
lations that characterizes the anadromous salmonids. In the long-term, this popula-
tion expansion is a guarantee against failure of a locale to provide for future needs.
In the case of tropical tunas, it explains their ubiquity in all the oceans.
The general messages delivered throughout previous volumes (Sharp and Di-
zon, 1978; Clark and Mangell, 1979; Sharp et al., 1983; Bard et al., 1998), and
this volume, are the described size-specific behaviors, aggregation phenomena,
and seasonal responses of tunas to oceanographic and biological production dy-
namics. Previous and present studies pinpoint the dynamic variabilities of the very
parameters in the fundamental biological simulation equations that Sibert et al.
(1999) have decided to hold constant. These include the highly variable and en-
vironmentally dependent catchability coefficient, aggregation size effects, and an
array of poorly estimated parameters regarding regional-seasonal movements.
Meanwhile natural mortality is allowed to float, as the main subject of study. But
mortality is not the quest in modem fisheries science-defining the basic charac-
teristics of the ecosystem that nurture survival and minimizing human interference
are the important issues (Sharp, 2000).
The value of large-scale tag-and-recapture experiments has been debilitated
by the well-known issues of reporting error. Over time, fishermen have learned
that various locations and environmental conditions induce more productive fish-
ing, depending upon the gear employed. The different gear types, deployed during
different times or seasons, create another suite of poorly accounted for issues in
the interpretation of tag returns, and inferences regarding fish behavior. This is
where archival pop-off (i.e., PSAT) tags are indispensable tools. With a lot fewer
assumptions, and a lot more ocean and location data available from both indi-
vidual fishes and aggregations of individuals, these dynamic resources will reveal
their true characters. Assuming that none of these dynamics exist to fulfill a wish
for convenient mathematical analysis is folly. Perhaps someday we will learn
enough to be able to credibly forecast these complex dynamics at realistic resolu-
tions. That, of course, depends upon there being good systematic observations of
the ocean, the fish, and fisheries. Tag dispersion experiments are only a small
fraction of the necessary information.
G. Disappearing Traditional Fisheries
It would be improper to leave out descriptions of gear types from some of the
old-world fisheries, as their disappearances are key to unraveling the continuous
changes in baselines used to manage modem high seas fisheries. Mather et al.
(1995) review the Atlantic bluefin fishery and biological information available
prior to 1977, with a few newer insights provided by more recent literature that
help dispel certain opinions about these fishes’ growth and development patterns.
One of the more informative summaries is their graphical depiction of several
regional fisheries, as sampled over periods ranging from one year to over two
decades. The most telling message of these regional graphs is the fact that there
were substantial size class modes of fish over 250 cm along the western Atlantic
from the Bahamas to Cape Cod and Ipswich Bay, Nova Scotia. These “giant”
tunas dominated the catch at Prince Edward Island, a famous sport-trophy fishing
ground. In recent years, these giants have declined dramatically in number, and
many new-generation tuna researchers have simply never seen a true convergence
of giant bluefin tuna (over 250 cm).
In the northeast Atlantic, off Norway, these giant fish contributed in some
years, but not in others. They were significant in the North Sea handline fisheries,
and appear in the rather typical adult fish distribution from the Spanish coastal
fishery. In the Mediterranean, the giant tuna occur in the Sicilian tonnara (traps),
and in the harpoon or “antenna” boat fisheries, two of the oldest recorded Euro-
pean fisheries. The giants’ most significant contribution was in the eastern Atlan-
tic/Mediterranean milieu in the Turkish Aegean and Black Sea fisheries. This
latter fishery ceased to exist in the mid-1970s, and most of the Spanish, Sicilian,
and Libyan trap fisheries have also declined to very low levels or have been aban-
doned. There has been a small recent resurgence in the Sardegnan trap fishery, but
there have been very few fish of true giant size classes.
The North Sea handline fishery was abandoned in the early 1960s due to its
complete failure. This and most of the older traditional fisheries declines can be
attributed to the combined effects of the emergence of the seine fishery off Nor-
way along with the North Sea handline fishery in the early 195Os, the advance of
Japanese longline fisheries in the Atlantic and Mediterranean; and the increased
French and Spanish seining activities along the eastern Atlantic and western
Mediterranean. In the recent decades there has been untold damage done to this
already stressed population by the clandestine roller-gillnet fisheries operated
from Sicilian or Tunisian ports.
With this somewhat longer perspective, it is clear that use of catch statistics
372 GARY D. SHARP
from the period from 1960 or so to the present yields a very pithy assessment of
what might be expected from less manipulated or debilitated populations. This is
a classic example of the continuously shifting baseline problem in the world’s
fisheries.
V. HABITS AND HABITATS OF TUNAS
Bard et al. (1998), in their excellent review of what has been learned in the two
recent decades, point out that laboratory and experimental research on skipjack
tuna (Kutsuwonus pelumis) was the benchmark or measurement basis from which
most of the original energetics-based conceptualizations about tuna ecophysiology
were derived (Sharp and Dizon, 1978). At the end of this earlier synthesis (Sharp
and Dizon, 1978), I was convinced that up until about age one, or about 40 cm, a
tuna was a tuna. All were alike in most ways. As laboratory studies have grown to
include other tuna species (see chapters by Graham and Dickson, Brill and Bush-
nell, and Farwell in this volume), differences between the species are still emerg-
ing, and help us to better understand their adaptations and behaviors.
Field observations provide the most applicable insights to help us dispel
dogma and tuna myths. These species have, indeed, carved up their environment
and thrive, often in the face of incredible odds. Josse et al. (1998) and Bertrand
et al. (1999a,b,c) bring the more holistic picture together by coordinating their
simultaneous observations of different tuna species movements, within a fully de-
fined acoustic survey environment. Yellowfin (Thunnus ahcures) and bigeye
(Thunnus obesus) seem to exhibit nearly opposite approaches to their shared en-
vironment. Yellowfin tuna spend their days making excursions from around the
top of the thermocline, both up and downward. Their nights are spent nearer the
surface, diving down into the emergent scattering layer to feed. Bigeye swim up-
ward from the cooler depths to stay with their food resources. These behaviors
seem to be keyed to the movements of the deep scattering layer (DSL). The day-
time deep-diving behaviors of tuna species are conveniently explained as a similar
response to food availability, and as a means of minimizing competition from
other upper ocean species.
One fundamental point is that skipjack (Kutsuwonus and Euthynnus) species,
as well as the longtail (Z’hunnus tonggol) and blackfin tuna (Thunnus atlanticus),
do not get “large,” as do other tunas. The longtail and blackfin tuna are tropical
neritic species with life histories otherwise more like that of skipjack, and they are
similarly limited in the adult size they can attain. This is not simply because they
cannot obtain sufficient food energy to maintain themselves and then pay their
unique metabolic costs of swimming, growth, and maturation-that is a truly cir-
cular argument. The concept emerged from an “Occam’s razor” interpretation of
the observation that maximum sizes increase and there are both greater ages and
larger sizes at onset of maturity observed, for example, in skipjack, arrayed from
the warmest to the cooler extremes of their upper ocean habitat. This is a generic
property that has been observed in many species from bacteria to hothouse plants,
as well as in coastal pelagic fishes where adequate data on growth, fat content,
maturation, and environmental time series are available (Mallicoate and Parrish,
1981; Parrish et al., 1985, 1986; Schulein et al., 1995). Thus the observed growth
differences could easily be a general result of available habitat temperatures as a
determinant of metabolic rates where somatic growth is traded off against higher
respiration rates. As well, there are the added complexities of food availability and
subsequent stress-related reproductive imperatives.
Another empirical corroboration is that it is not uncommon to find skipjack of
90 cm (over 20 kg) in the eastern tropical Pacific south of the equator. Skipjack
of such large sizes are virtually unheard of west of the international date line in
the Warm Pool. Yet, swimming in abundance in the great depths of the Warm Pool
region, where the 23°C isotherm may lie as deep as 450 m, large (> 100 kg)
yellowfin and bigeye are common. Albacore (Thunnus alulunga) also occur, but
are less abundant than in the adjacent regions to the north and south of the Warm
Pool, or east of the date line (Parrish et al., 1989). Here, again, we see another
dichotomy. Skipjack, yellowfin, bigeye, longtail, blackfin, and albacore are ca-
pable of extensive overlap throughout their adult lives within the environments
that support their egg and larval stages. Yet the adults of these species have
parsed out the broad ocean environment, using temperature extremes, habitat, and
vertical and latitudinal partitioning of food resources as major habitat-defining
properties.
Relatively puzzling, the above information considered, is the odd ecological
position and resulting behavior and physiology of albacore when compared with
the other Thunnus species. Beyond the relatively small amounts of red muscle and
long pectoral fins, these fishes have unusually numerous hemoglobin forms,
and many “unique” proteins, unshared with other Thunmds (Sharp and Pirages,
1978; Collette, Reeb, and Block, this volume). Albacore start life in much the
same way as do bluefin tunas, with extensive juvenile migrations from their natal
habitats in the equatorial ocean into subtropical ocean waters (16-20°C). Then as
they grow and mature, they submerge into the well-oxygenated middepths of the
tropical latitudes. Few, if any, adult (>95 cm) albacore occur in surface fisheries.
Longline-caught adult albacore from the Atlantic, Pacific, and Indian oceans can
obtain relatively large sizes (to over 130 cm), but never the extremes attained by
the yellowfin, bigeye, or three bluefin tuna species [i.e., Pacific bluefin (Thunnus
thynnus orientulis) and Southern bluefin tuna (Thunnus mccoyii) to 150 cm and
Atlantic bluefin tuna (Thunnus tizynnus thynnus) to 250 cm or more]. The expla-
nation for why albacore do not also get larger remains open. They differ in several
other ways.
For example, tagging studies of tunas are numerous, and although many al-
374 GARY D. SHARP
bacore have been tagged, very few have been recaptured (less than l%), in con-
trast to other tunas where recaptures can run as high as 10%. Explanations are
many. Tagging mortality may be very high. Anecdotally, albacore fishermen
nearly always remark about the fact that they must slow down their boats while
trolling jigs, or the hooks tear out of the mouths of the juvenile albacore that take
their lures. The greater impacts due to higher trolling speeds ordinarily cause other
juvenile tunas to pop up to the surface and plane long before the hooks would cut
through their jaws. Also, when fished with pole and line, albacore seem to have
“soft mouths.” and many are lost off the hooks, compared with other tunas.
Similar-sized skipjack, bonitos, mackerels, and all the other tunas seem to be more
durable and tougher. Aquarists have had problems keeping live albacore, too,
while most other scombrids have proven to be hardy in aquaria (C. J. Farwell,
personal communication).
Bach et al. (1996) made a study of albacore using experimental longlining
research techniques similar to those developed by Boggs (1992), and described in
full by Abbes et al. (1999). They found that the albacore catch-depth positions
were not different from those of large yellowfin (warm water) but significantly
different from bigeye typically found at cooler depths. Catch rates from longline
sets made at different times of day also varied in response to the unique patterns
of night and daytime swimming depths exhibited by each species, with albacore
acting more like yellowfin. Bard and Josse (1996) have documented another of
the unusual distinctions that may contribute to the albacore’s general fragility rela-
tive to other tunas. They noted that when the albacore were brought on deck, they
were usually bleeding from the gills or throat, and were dead or died quickly,
rather than flapping about like other tunas in the catch. In further examinations
they discovered that this was due to ruptured gas bladders. This phenomenon was
not observed in other tunas from the same catch. This relatively fragile organ in
albacore might help explain their intermediate location within the water column
and ecological milieu.
Although the adult albacore’s niche seems to lie within the range of adult yel-
lowfin, and overlap with young bigeye, as juveniles they appear to thrive best on
the transitional fringes of the subtropical ocean (from about 16 to 20”(Z), where
bluefin are the only potentially abundant thunnid competition. Juvenile migrations
of both species can be notoriously long, but the habitat preferences of adult alba-
core seem to be more tuned to the middepths of near-tropical ocean than those of
the bluefin. The southern bluefin may be the only exception. The two species
appear to overlap at the warmer end of the juvenile bluefin habitat, with the alba-
core being slightly more abundant in the adjacent subtropics until the older adult
southern bluefin begin their spawning migrations into specific warmer ocean re-
gions with tropical SSTs.
The three bluefin species seem to spread themselves out across the subtropical
to temperate oceans, aggregating seasonally at the productive subtropical to tem-
perate ocean convergences as juveniles. The adults are hardy and cold tolerant.
Although they can foray into deeper tropical to temperate environments, they
spend most of their nighttime at the surface in warmer waters where temperatures
range from 9 to 23°C or so. From the surface layer they forage to depths of over
1000 m. This is a generality (Gunn and Block, this volume), and southern bluefin
(Farley and Davis, 1998) seem to key into warm, productive surface waters to
spawn. It also appears that the southern and Atlantic bluefin, like the tropical tu-
nas, are serial spawners (Hunter and Goldberg, 1980; Hunter et al., 1986; Schae-
fer, 1998; Farley and Davis, 1998), provided that they enter the spawning areas in
good energetic states, and then find accessible forage. Without local forage, they
likely leave local, particularly warmer environments to recharge depleted body
fat, as Sharp and Dotson (1977) reported for juvenile albacore.
Adult bluefin tunas are obliged to enter tropical environments, as do all tunas,
that are not apparently best suited for their growth and maintenance in order to
situate their eggs and larvae in amicable locations. Larval tuna survival environ-
ments need adequate food resources and minimal predators. This basic obligation
is likely the key to their relatively smaller numbers and erratic spawning successes
compared to the more ubiquitous skipjack, yellowfin, and bigeye, and even the
“fragile” albacore. The bluefins’ late maturation and immense adult sizes provide
several advantages over the tropical tunas. They can tolerate and operate in a
greater range of ocean conditions; they can store more energy to be used in repro-
duction; and they can carry huge numbers of propagules to invest in short-term,
local spawning events. The burden is that they must survive longer, within a
broader, if perhaps less competitive, subtropical milieu while growing into their
adult form and full reproductive capabilities.
The Mediterranean provides a full suite of seasonal options for the Atlantic
bluefin, with seasonal warm surface water spawning areas distributed across the
northern and eastern extents, overlaying cooler habitat. The year-to-year environ-
mental variability in the Mediterranean Sea creates another source of variability
for these fishes’ early life stages to cope with. While their well-dispersed life-
history phases are clearly “Darwinian” survival tactics, the adults appear to con-
verge and congregate in small size-similar groups for localized spawning. What is
obvious from the catch by size graphs in the Mather et al. (1995) historical review
is that the variously located bluefin tuna fisheries each interact with a unique frac-
tion of the total population. It also appears that there is a form of “homing” or
repeat performances as these size cohorts wander about the Atlantic and enter
various gamuts of fishermen.
Also apparent from these data sets is that eastern Atlantic coastal and Medi-
terranean fishery catch numbers tended to peak every 5 to 7 years. From the
Mediterranean and Atlantic trap fishery data, the bluefin cohorts converged from
both north and south, each with unique catch and fish size patterns (Mather et al.,
1995). Once inside the Mediterranean, intermediate recruitment peaks could be
376 GARY D. SHARP
seen as arising from these different cohorts, suggesting that there were some
physical reasons, as well as some age-specific behaviors, that tended to create
apparent cycles. Today, due to the reduction of breeding populations and “crop-
ping” of age classes, fisheries that focus on either their seasonal feeding or spawn-
ing migrations pose the single greatest threat to their survival.
In capsulated form, bluefin tunas become more capable opportunists as they
grow, being able to explore and exploit more voluminous and heterogeneous habi-
tats as they search for nutrition. As adults, they can process and store massive
amounts of energy that is then used to travel in search of the right places to deposit
their stored energy as investments in a next generation. The dichotomy is that the
tropical tunas invest more frequently, within a less varied and broadly dispersed
milieu, supporting generally larger populations, while the bluefin tuna populations
undergo extreme oscillations, based on smaller populations, exploring an even
more vast environment. Both strategies work. The latter is adaptive to long-term
climate variations, but is more susceptible to human intervention when popula-
tions are small.
Clearly, the broad and nearly continuous distributions of the several Thunnus
species is an odd situation that is difficult to explain in usual zoogeographical
contexts, often defined by specific temperature and food preferences. Specific de-
velopmental characteristics of each species delimit the various life-history stages,
by species, in the ocean continuum. It is also clear that the tunas’ general ten-
dencies to aggregate about mammals and large sharks, topographic features, or
other “objects” (FADS)-as well as within the convergence-mediated patches of
plankton-create the concentrations that fisheries are dependent upon. Develop-
ing insights into these aggregation associations has been slow, beyond their acting
as “feeding stations” (see Boggs, 1996, for a review of prior behavioral research).
As Sharp (1978) pointed out, prediction of precisely where and how many tunas
there will be is not feasible, but projections of where and when tunas will be
vulnerable is important, and can be learned by carefully planned and executed
research programs.
VI. COORDINATED EMPIRICAL STUDIES

OF TUNA BEHAVIOR AND ABUNDANCE
WITHIN OCEAN GRADIENTS
The importance of systematic and coordinated research methods emerges as

the next requirement for the integration of basic research projects with fisheries and
environmental time series information before our task is completed. Recent re-
search from the ECOTAP (Etude du Comportment des Thonides par 1’Acoustique
et la Peche; Abbes and Bard, 1999) study based in Tahiti provides good examples
of careful project planning, execution, and analysis needed to document the be-
haviors of several tunas within a complex environment of both narrow and broad
gradients. Having reviewed the recent ECOTAP literature, including several pos-
ters that they have produced for various recent meetings, I applaud the scope of
their efforts. They set out to learn about the potential for a new longline fishery in
the region of French Polynesia. A rigorous, vigorous, and yet practical research
program was planned and executed. Through multivariate statistical approaches,
and carefully stratified simultaneous observations, they have generated a useful
understanding of how these species respond to and share the resources across a
large region of the world’s ocean. From the coordinated measurements of physi-
cal, chemical, and planktonic production, they have developed insights about the
tunas’ relative distributions based on their different physiological limitations.
Yellowfin tuna are caught on longlines throughout the region, from 50 to
350m, except in the very northern extent where low oxygen levels at depths of
about 200 m preclude their presence below that level. A few degrees to the south,
they fully occupy this depth range. Overlying all of this is a “layer” of skipjack
tuna and other small- to medium-sized surface-oriented predator species coexist-
ing and competing for resources in the upper ocean. As the skipjack grow, they
reach deeper into the habitats shared by these larger tunas. Because of the shallow
strata of plankton-induced oxygen depletion in the north of their study region, and
warm surface temperatures above 100 m, albacore are excluded from the surface
and less oxygenated depths. Albacore are present wherever the low oxygen and
<26”C SST phenomena do not intersect, and their relative abundance increases
toward the south to at least the 450-m depth limitation of the researcher’s observ-
ing systems. Bigeye occupy the full range, but are situated between 250 and 550 m
at 2O”S, and their habitat’s vertical dimension decreases systematically toward the
north, such that between 4” and 6”S, they occupy the water column between 100
and 250 m, overlapping the bottom portions of the skipjack, yellowfin, and alba-
core habitats.
Available temperatures, per se, in this region do not pose critical limitations
for any of these species. The combined effects of oxygen, food abundance, and
seasonal changes create this dynamic interaction. When the ECOTAP observa-
tions of micronekton abundance were plotted along a southwest-oriented transect
from 11” to 14’S, Bertrand and Josse (1999) found that the micronekton were
concentrated in a weak convergence zone. As expected, to the north they found
that remineralization caused oxygen depletion below the shallow mixed layer. To
the south, oligotrophy limited micronekton growth and distributions. Thus, they
described the food production distribution within their study area. Their study
took place from 1995 to 1997, a period of extended low Southern Oscillation
Index and frequent ENS0 Warm Events, creating an alternative scenario to that
expected from earlier observations made by previous researchers.
378 GARY D. SHARP
The participants in the ECOTAP program focused on several specific subjects

that are brought together in the end to define their integrated research strategy.
Their first objectives were to test the efficacies of hydroacoustic tools in identify-
ing the behaviors of micronekton, the food organisms that attract tunas to all the
documented ocean fishing regions (Blackburn, 1968; Carey and Olson, 1982; Ol-
son and Boggs, 1986; Marchal et al., 1993; Roger, 1994; Roger and Marchal,
1994; Bertrand et al., 1999). Next came the problem of in situ location and iden-
tification of individual tunas, in order to explore their interactions and unique
behavior within the larger system.
The next subjects needing exploration were methods to approach and resolve
the fine-scale behaviors of the region’s tunas, within their constantly changing
milieu, and all within the larger context of regional oceanic gradients and their
dynamics. Recognizing that longline catch rates poorly reflect abundance or dis-
tribution when the hooks do not cover the entire habitat (Hanamoto, 1987), ECO-
TAP scientists carried out acoustic studies to locate and identify the three impor-
tant tuna species in the region. Bertrand et al. (1999) caught, measured, and
attached ultrasonic tags to several yellowfin and bigeye tunas in order to track
well-identified individuals while using a split-beam echosounder to measure their
individual target strengths and behaviors. They could not, however, discriminate
between species using these tools, posing a challenge regarding species-specific
behavioral or abundance information. They verified the utility of the split-beam
echosounder in tracking individuals, despite variations in target strengths as each
fish changed orientation and swimming behavior. The above dilemma and related
problems need to be resolved, especially if seeking answers to questions about the
distributions and behaviors related to developmental state, size, and sexual status
of the several species.
The ECOTAP team produced a reasonable and clear picture of the oceanic
habitats of the three tunas of greatest importance to the region’s longline fisheries,
as they set out to do, and then delivered their results into the real world as Tahiti
and French Polynesia endeavor to develop and enhance their longline fisheries. I
should make it clear that these are not the first acoustic tracking studies of this
type, but they do represent uniquely full-featured simultaneous oceanic tracking
of more than one species, without the interference of local island or topographi-
cally forced dynamics. The ocean fisheries helped define their research plans. This
is “system science,” long the focus of my personal objectives.
The first stage in development of all rigorous tuna behavior studies has been
to refine the local-scale observations such that they give you fine detail on the
behaviors of the fish with respect to identified features or structure(s) in the water
column (Boggs, 1992; Holland and Sibert, 1994). Bach et al. (1998) have sum-
marized previous and ongoing FAD-related tuna behavior studies. They con-
cluded that their acoustic survey tools would also need to be improved so that they
could be used to cover greater depths and wider horizontal areas, a problem com-
mon to most tuna FAD research to date. As previously discussed, small bigeye
often mix in with FAD-associated skipjack and yellowfin schools in the seine fish-
ery in the equatorial eastern Pacific. Without the influence of the FADS, bigeye
are usually found at great depths during daylight hours, with occasional forays
into the warmer surface layers. Dagorn et al. (1999) followed four medium-sized
(25 -50 kg) bigeye for periods ranging from 6 to over 30 h each. The fish traveled
very different distances during the tracking periods, covering 25.5 km in a 6-h
track and over 106 km in a 33.5-h track, and ranged from 10 to 60 km from the
point of origin (demonstrating the point that tunas are not “advection” analogs,
but actively search their habitats at speeds that far outrun internal ocean dynam-
ics). These fishes and all active swimming species must be treated as volitional
and motivated predators.
Bach et al. (1998) tagged several small (48-60 cm) yellowfin-some near
and some away from FADS. In tracks of over 48 h, they describe results similar to
Josseet al. where the small yellowfin made forays to 250-m or greater depths from
the surface layer. The FAD-associated fish ranged to depths from 175 to over
250 m during the day, with short forays to over 400 m. At night the fish rose nearer
the surface, wandering about between 50 and 250 m. Brill et al. (1998, 1999)
described similar sonic tagging experiences off Hawaii, for both small and large
(45 to 90 cm) yellowfin, and found that they tended to stay in the uniform surface
layer. Comparing these results with those from the more open ocean tracks, and
those with simultaneous acoustic plankton survey data, there is clearly more to
studying tuna behavior than only focusing on their specific temperature and oxy-
gen needs. The greatest frustration with these labor-intensive sonic tagging studies
is that they tend to be relatively short-term, that is, most less than 24 h. Fortu-
nately, the newer archival tagging technology has provided means for obtaining
verification over extended periods of these fishes’ behaviors. There is also the
more realistic perspective of changes in die1 behaviors in response to environmen-
tal conditions as the fish exploit features and move from region to region (Holland
et al., 1990, 1992; Dagorn et al, 1999; Gunn and Block, this volume).
There are certain advantages that studies within the larger ECOTAP region
(Abbes and Bard, 1999) and basinwide archival tagging studies (Gunn andBlock,
this volume) offer over more localized island or FAD-based studies. These include
the movements within long-scale linear gradients and large-scale ocean processes
within which these fishes operate as individuals, species, and competitors-in
contrast to the local feature basis of island or sea mount attractions within either
seasonal migrations or seasonal shifts in latitudinal current patterns. Both local
and open ocean studies have their place, but the fine-tuning of our understanding
depends heavily upon learning how these species operate within a common mi-
lieu, and how they partition themselves as they grow and develop the many special
adaptive strategies that each has evolved.
380 GARY D. SHARP
VII. TUNA SCHOOLS AND

DYNAMIC INTERACTIONS
To fisheries managers, abundance is the question. To fishermen, efficiency is

the question. To physiological ecologists (and the fish)-given the continuous
changing habitat conditions-the spectrum of behavioral responses and species
specific developmental stage-wise adaptations hold the answers. One such ques-
tion that has significance to population abundance assessments and fisheries pro-
duction is that of the dynamics of tuna school sizes, as measured by fish landed
within a single set of a seine net, or independently, from acoustic information. The
main reason that FADS are used is to concentrate fish from relatively sparse abun-
dances, as described above for the large tunas. The dynamics and interactions of
the aggregations require special consideration, for several reasons. The need for
careful analysis including environmental information is to alleviate the dichoto-
mies that result of simplistic conceptual models where only one parameter is used
to define changes in relative abundance, vulnerability, and all the non-fisheries
density related interactions.
Sharp (1978) and Sharp et al. (1983) described why it is nearly impossible to
distinguish between changes in availability and changes in abundance without
good records of both measures of habitat situation and catches by size/age groups.
Superschools are observed to form and break up in time around most of the ob-
jects that have been observed to aggregate tunas. The reason for these associations
is still poorly understood (Dagom and Freon, 1999). My early studies (Sharp,
1978) showed that school sizes tended to be larger where the available habitat’s
vertical dimensions were narrowest, suggesting that there is a relation between
local fish school densities, encounter rates, and school or aggregation size. The
modal small school was about 7 tons, although smaller schools would not be set
upon in most circumstances in today’s ravenous seine fishing environment.
Bertrand and Josse (1999) continued the study by surveying bigeye abundance
in the study region, finding about 1.33 fish per km2, or 33.8 kg bigeye per km2.
They also measured tuna densities around FADS, and found 3.65 fish per km2. In
a comparison with IATTC stock assessments, within a well-fished region, they
found that IATTC estimates showed an average density of 0.83 fish per km2. Thus,
they confirmed my original statement (Sharp, 1978) that “if tunas were truly uni-
formly dispersed in their habitat they would be so rare as to be virtually nonexis-
tent.” They were also able to confirm that their acoustic techniques “allow obser-
vation of such ‘virtually nonexistent’ tuna.”
A. Why Tunas Aggregate
The largest recorded single seine set capture in the early (pre-1976) IATTC
logbook records was a 200-ton skipjack school, aggregated on a piece of discarded
9. TUNA OCEANOGRAPHY-AN APPLIED SCIENCE 38 I
hawser. Typically, the catch from individual fish schools taken in the early seine
fisheries followed a negative binomial size distribution. Years of observations
aboard fishing vessels show that smaller free swimming tuna schools tend to be
more size homogeneous. As the school size increases, there is a clear increase in
size range, multiple size-age modes, and often mixed species. In yellowfin ge-
netic studies (Sharp, 1978), larger schools with mixed size/age classes have
tended to comprise more than one genetic unit. Clumps of similar-sized individu-
als with rare alleles were observed in schools that were sampled for either size-
related differences (broad size ranges) or very narrow size ranges, suggesting life-
long cohesion as a result of fish size similarity (Sharp, 1978). There is apparently
an inherent need for same size fish to maintain coherence.
Bonabeau and Dagorn (1995) began by looking for universal principles for
fish school size distributions. Because of the sampling problems, tuna school size
dynamics remain a mystery (Bonabeau et al., 1999). Clark and Mange1 (1979)
and Clark and Mange11 (1984) showed that if there were a habitat-mediated con-
centration effect, it could severely bias abundance estimates based on catch per
unit effort statistics. In fact, as discussed above, the entire aggregation phenome-
non needs to be better understood, including some intense efforts to study the
coherence of various schooling structures, from small size-similar schools to mul-
tispecies aggregations. The studies need to be done in the open ocean rather than
only in areas where FADS or island phenomena dominate the situations.
VIII. THE IMPORTANCE OF STUDYING

INDIVIDUAL FISH BEHAVIOR
Electronic archival tags are among the many new tools that allow us to study
individual fish behaviors over extended time and space domains. The pop-off ar-
chival satellite tag (Block et al., 1998; Gunn and Block, this volume) offers the
greatest variety of synoptic behavioral and environmental data collection. There
are relatively large amounts of life-history and migration data derived from de-
cades of tuna tagging (Bayliff, 1996) and returns from fisheries catches. There is
only a modicum of behavioral data from sonic tracking of tunas. Most of these
data were collected within the coastal and fisheries environment for a few hours
to a few days. However, longer records of the movements and migrations of large
numbers of fisheries-independent tunas, and the study of their daily behaviors in
different environments under different modes of behavior (traveling, feeding,
spawning, etc.), have yet to be collected in sufficient quantity, but vast amounts of
new information are now being acquired.
It is tempting to make the leap from the fisheries catch information to their
more complex behaviors from a few small examples, but the complexities of
schooling, population structure, and breeding units remain to be understood
382 GARY D. SHARP
(Sharp, 1978). Without exaggerating, it is simply imperative that more systematic

research into these topics be undertaken. The history of the development of the
archival tag and the transition from implants to the pop-off satellite generation
have been slow until just the recent few years, when the various researchers in-
volved began to home in on the differences between anecdotal data sets and
replicate-rich, but expensive, tagging efforts. All of the recommendations from
the recent reviews of tuna fisheries interactions include enhanced tagging efforts.
But I would suggest that there is no more valuable information than that derived
from archival pop-off satellite tags, given the problems with reporting, tag shed-
ding, and our ignorance of age-specific behaviors of most all of the tuna species.
Whatever moneys are being spent on distribution and mixing studies is being
short-circuited by individuals or corporations with opposing agendas.
Again, the differences between FAD- and island-associated research have be-
gun to emerge, telling us that “local” feeding behaviors and growing phases of
tuna migrations are distinct from their behaviors during the traveling and disper-
sive phases (Block et al., 1998; Lutcavage et al., 1999). The differences associated
with traveling and dispersion behaviors are likely associated with seasonal and
interannual oceanographic processes, as well as experience gained as each cohort-
unit explores the larger habitat available to them, if so motivated. One can quickly
surmise that a fish or group of like-experienced and similar-size individuals that
find themselves located within a food-rich, amicable environment will not be as
likely to move on into a less productive environment as those fishes in regions of
limited food.
IX. THE ECOCOSMOLOGICAL QUESTION:

“WHY ARE TUNAS WHERE THEY ARE?”
The answer is simply, “because they can be there.” At evolutionary extremes,

bigeye and albacore tunas offer good examples of life-history patterns that have
succeeded to varying but lesser degrees in accomplishing the niche expansion that
has been more completely attained by the bluefin tuna group. They have adapted
similar strategies, but accomplished different capabilities. The trade-offs in ulti-
mate adult size, longevity, and propagule delivery capability are complex, difficult
to evaluate measures of survival tactics, and should be carefully considered when
theorizing about relative productive potentials and likely recruitment successes.
As forecasts are the ultimate objectives of science, credible fisheries recrnit-
ment forecasts are the Holy Grail of fisheries oceanography. The designing of
research into conditions promoting, or not, the survival of various life-history
stages of tunas has only just begun to deal with local environments. The seasonal
cycles within the oceans are of greatest impact on these processes. We also now
know that interannual variability and decadal scale regime shifts tend to create the
more large-scale dynamics that make it imperative that we not get trapped into the
idea that every year produces the same recruitment expectations. This fuzzy as-
sumption has been a major failing of recent fisheries management as a product of
model-dominated parameterized science over observation-driven science. These
are not new issues (for reviews see Sharp, 1981a,b, 1995) but they do get in the
way of progress and precautionary management of poorly understood resource
species. There is a lot more systematic science needed to done. The combination
of archival tagging, ocean observations, and ecological monitoring is the only
available solution to the remaining dilemmas, presuming that they are embedded
within the matrix of continued collection catch and effort statistics, and better
pinpointed catch locations, within a more realistic temporal and spatial framework
of synoptic measurements.
Recruitment successes are “events” resulting from the intersections of many
rare and unlikely phenomena, and many normal biophysical interactions and pro-
cesses. Mostly, these are not subject to mean and variance or equilibrium system-
based statistical procedures (Lasker, 1975; Hunter and Goldberg, 1980; Sharp,
1981a,b). Credible predictions of future recruitment survival patterns can only be
usefully accomplished from individual (species and size) based modeling perspec-
tives and thorough understanding of survival requirements for each subsequent
life-history phase. This does not preclude forecasts for larger regions and major
phenomena such as ENS0 variations of simple species-specific recruitment re-
sponses such as above, below, or about some longer-term mean responses, par-
ticularly for mast tropical tunas, and even some of the cold-water tunas.
Our principal ecological problems still lie with understanding species distri-
butions and aggregation-size behaviors and relationships. Recognizing that the
temperate tunas live in a poorly understood, dynamic and inhomogeneous do-
main, their behaviors are apparently more opportunistic (exploratory). Where they
might be located at any time likely depends upon their individual or group expe-
riences within these more dispersed features, structures, and processes, enabling
them to locate food resources and grow to adulthood. Even more complex issues
must be resolved for their reproduction to be successful. Combined, the where and
when solutions are subject to physically driven ecological responses, life-history
stages, experience, and additional constraints posed by fishing pressures.
Attempts at environment-free statistical population forecast models will cer-
tainly continue to fail, as they have done for most long-lived fishes, for the same
reasons. The tunas are not alone in creating this dilemma, as many species with
fine-scale requirements within limited, environmentally “noisy” habitats need to
contend with similar problems. The common denominators of these species in-
clude longevity, migratory dispersion, large adult size, and immense investments
in propagule deliveries and distribution (sometimes even live-bearing), and their
combinations, as means of resolving the temporal and spatial inhomogeneities for
their young. Most adult fishes are mobile and responsive to most ocean situations.
384 GARY D. SHARP
With this perspective, the increased study of individuals is certainly appro-

priate if we are ever to truly come to comprehend how these many species
have succeeded in carving up the world’s oceans into such overlapped habitats.
Through species-specific physiological adaptations, morphological accessories
such as their individualized circulatory plans, and their sometimes shared, some-
times unique biochemical capabilities, tuna species have adopted adaptive behav-
iors that operate across most of the upper ocean, to at least 800 m, between the
bounds of the polar oceans. They are not alone, as they are feeding alongside
marine mammals and other large, widely dispersed denizens whose life histories
are also cryptic and only available for study using the new digital archival tools.
X. CONCLUSIONS
These many anecdotes make the point that tuna oceanography is both an im-
portant applied science and an essential economically relevant activity. The direct
applications of knowledge about species distributions, interactions, and behav-
ioral responses to environmental processes and patterns are useful from the earli-
est stages of fisheries development into the expansion phases that have character-
ized most ocean fisheries. As well, the insights that well-measured ocean patterns
and changes provide are crucial to the longer-term responsibility of managing and
nurturing these highly mobile, renewable resources. Where I have advocated that
fishing vessels be incorporated into the tasks of environmental monitoring, it is
clear that the fish themselves now offer even more opportunities, as they become
integrated into the observation systems, to provide synoptic information about
their own forays within their vast array of options. The emergent archival tag
technology, particularly the PSAT archival tags, provides new ways for all ocean-
ography to become better applied, and ever-larger perspectives on fishes and
oceans to emerge. There are few or no better uses of ocean science funds than to
attend to these issues.
Ultimately, the likelihood of success in managing exploitation rates of fish
populations with the primary objective of maintaining them in perpetuity depends
upon the integration of information about individual self-sustaining population
units and their interactions with competitors within the constantly changing eco-
logical milieu. This is the realm of “applied physiological ecology,” and includes
careful study of physical ocean and atmosphere variability as a basis for interpre-
tations. This necessary understanding can only arise from carefully thought out,
systematic studies of the oceanographic and ecological milieu, that is, the target
fish species, their ecological interactions, and the various aspects of each fishing
gear type that promote their success, or not. This is “fisheries oceanography.”
These two applied science topics are how and where empirical scientific knowl-
edge is applied to the management and optimization of all the fisheries interac-
tions, with the objectives of sustaining all living resources and the humans who
are dependent upon them. These objectives are clear. The politics are often more
obscure. The challenge is to continue to gather observations in order to continue
to learn and then better apply what is known toward these objectives. It is an
exciting time now that we have the tools, and a critical mass of concerned tuna
scientists.
ACKNOWLEDGMENTS
1 am first and foremost dedicated to the best interests of the fish and fishermen. If applied wisely,
the science that I perceive as being most noteworthy is an important means of ensuring the survival of
both. Everyone who has been involved in this difficult research deserves credit for their diligence and
foresight in their efforts to resolve important problems in basic ecology, applied science, and fisheries
conservation. First Davy and then Kishinouye, followed by John Magnuson, Frank Carey, and Bruce
Collette-from their works came the insights that sequentially got many of us interested. Meanwhile,
Luis Rivas, Rodriguez-Roda, and Frank Mather III kept our sights on why, and for whom, we do our
science. Recent progress has been remarkable. In my experience, there are many who forget that we
are allowed to do our work for reasons other than filling library shelves, or resumes. The world’s
fisherfolk need our answers now, if not yesterday. It is ah about the future. I thank Andre Boustany for
reading an early draft and helping me to sift and order the original draft so that those who are learning
about tuna biology, ecology, and oceanography for the first time might keep a common thread as they
read what I have written. To Don Stevens and Barbara Block, whose patience and efforts over the
recent decades have been remarkable, I thank you. 1 can only hope that as a recognized poser of tough
questions, and a general skeptic, those whose efforts I have not highlighted will forgive me. All sincere
efforts are appreciated, and all information shared is cherished.
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10
TUNAS IN CAPTIVITY
CHARLES J. FAR WELL
I. Early History
II. Tunas in Captivity
A. Commercial Tuna Farms
B. Captive Tuna Research Facilities
III. Aquarium Displays of Tunas and Related Species
IV. Methods of Collection and Care
A. Collection
B. Captive Care of Tuna
C. Handling Techniques
D. Growth
V. Research Opportunities with Captivr Tunas
VI. Future Efforts
I. EARLY HISTORY
Members of the Family Scombridae have captured the attention of humankind

for millennia. In this chapter I examine how captive populations of bluefin tuna
have been maintained. Included in the History of Animals (Aristotle, 2350 B.P.)
are detailed descriptions of the Atlantic bluefin tuna, Thunnus thynnus, and their
annual spring migrations to spawn in the Mediterranean Sea. Pliny (1950 B.P.)
chronicles a description of vast schools of tuna impeding the forward navigation
of Alexander the Great’s fleet (Butler, 1982). Bluefin tuna were highly valued for
food throughout their history with man and elaborate undersea traps were built
and maintained for the purpose of catching tuna. The earliest traps were set by the
Phoenicians over 3000 years ago and evolved into the specialized traps called
“tonnara” used today (Butler, 1982; Maggio, 2000). These traps have been used
throughout the Mediterranean from Spain to Turkey and into the Bosporus. To aid
in catching tuna, the Romans and the Greeks built watchtowers specifically for the
purpose of sighting or locating the migrating tunas. Early Roman cities, such as
Baelo Claudia, 200 B.C. (Bologna, Spain), were built in coastal areas for the com-
391
Tuna Volume 19 Copyright 0 2001 by Academic Press
FLSH PHYSIOLOGY All right? ofrepraducr~on m any form reserved
392 CHARLES J. FARWELL
mercial trade of catching and salting tuna. The practice of using tonnara to catch
bluefin continues today, primarily in Spain, Portugal, and Italy, although only a
few of the tonnara remain in use. Mediterranean Sea traps were set to catch giant
bluefin in a short period of time. The flesh would be canned, salted, or preserved
in olive oil for future use. Once empty the traps would be hauled out of the water,
mended, and reset for a new catch, repeating the process until the migration had
run its course.
The importance of tuna to early civilizations living in this area is captured
by the drawings of tunas appearing in Italian cave paintings dating back 4000
years B.P.; images of tuna on Phoenician coins date back to 2500 years B.P. (Butler,
1982) and on pottery vases depicting the bartering over tuna from 2400 years B.P.
(Maggio, 2000). In other areas of the world, shell mounds containing skeletal
remains of Thunnus species have been found, indicating they were a part of the
early diet of humans. Thunnus bones date from the early to middle Jomon period
of Japan, 6000-4000 years B.P. (Komiya, 2000), and in coastal areas of British
Columbia from 3000 years B.P. (Crockford, 1997). This leads to the conclusion
that the value of tuna, revered both as food and for its beauty, was appreciated in
early times and universally sought by many cultures.
II. TUNAS IN CAPTIVITY
A. Commercial Tuna Farms
1. CANADA
The first use of anchored, floating net pens for commercial use to hold bluefin
tunas for extended periods of time occurred in 1975 at St. Margaret’s Bay, Nova
Scotia, Canada. The original idea was to hold the tuna for an extended period of
time, allowing the tuna to be sold at a time when market forces would bring a
higher price for the fish. Giant bluefin tuna were captured during the summer
season when they migrated into Canadian waters. Feeding the impounded tunas
over the holding period had the added value of increasing the size, weight, and oil
content of each tuna, thus generating a greater monetary return. The first pens
were engineered and built by Japanese technicians; they were attached to mackerel
traps by means of a tunnel made of netting which could be opened and closed so
the tuna could be moved from the traps into the holding pens (Buchanan, 1977).
The original impoundment consisted of eight pens that could accommodate a total
of 600 tunas with an average mass of 500 kg each. The nets used in the impound-
ment were oval in shape and measured 100 by 50 m and were 15 m deep (Bu-
chanan, 1977). The early success of the Nova Scotia bluefin tuna impoundments
started a worldwide effort at duplicating their efforts.
Today there are tuna ranches or farms throughout the Mediterranean Sea, Ja-
10. TUNASINCAPTIVITY 393
pan, Australia, and Mexico. All three bluefin tuna species are currently involved
in farming operations. Collection of tuna for the farming operations in the Medi-
terranean area, Mexico, and Australia rely primarily on tuna caught by purse
seine. The seined tuna are transferred to a tow-pen, which is approximately 45 m
in diameter and 15 m deep. Once the tunas are captured the tow-pen is slowly
brought back to the central holding pen area at a speed through the water not
exceeding 1 knot. Transfer of the tuna is accomplished by mating the tow-pen to
the holding pen and driving the tuna through the common opening.
2. MEDITERRANEAN
In recent years in the Mediterranean, Atlantic bluefin tuna penning has in-
creased and operations vary depending upon the target size of the bluefin. Pens
are found currently in Spain, Italy, and into the Adriatic Sea, as well as other
Mediterranean countries. Penning operations, focused on juvenile fish start in late
winter to early spring and run through to fall; the sizes are mixed, ranging from
15 to 40 kg, and 2 to 4 years of age. Penning of giants accounts for a significant
amount of the quota being taken in Europe. For example, in Spain 7 farms or pen
operations with a combined total of 45 pens hold a capacity of 6000 mt (metric
tons). Italy has 1 pen operation. Croatia has 5 farms with a total of 17 pens of
unknown holding capacity. Traditional traps are found in Spain, Sicily, Portugal,
Morocco, and Tunisia. Fishing effort for bluefin to be held in traps and for stock-
ing the pens is timed to coincide with the spring migration of the giant tunas that
come into the Mediterranean Sea for the purpose of spawning during the summer
months. Harvesting from the pens frequently extends throughout the year and into
spring of the following year, and the tuna are sold either as fresh or quick-frozen.
The traps are harvested as they fill with fish; the fish are removed, slaughtered.
and prepared for shipping to market.
3. AUSTRALIA
Australian tuna farming focuses on the southern bluefin tuna, Thunnus mac-
coyii. The primary location for the operations are in the Port Lincoln area of south-
ern Australia. It is the largest of all tuna farm operations with as many as 100 pens
with a starting mass of approximately 5000 mt and a harvest mass of 7000 mt in
2000. The dimensions of the pens in Australia are the standard used by the other
farms and have their roots in the original impoundments of Nova Scotia. The
southern bluefin tuna are collected seasonally during the Austral summer months
in the Great Australian Bight. The average age and size at the time of collection
is 3 years old and 20 kg mass (Glencross et al., 2000). After being transferred to
the farm pens they are maintained for up to 8 months and fed a diet of sardines
and a commercially available product called “wet pellets” (Glencross et al.,
1999). Maximum growth occurs during the summer period of warmer water, 17-
394 CHARLESJ.FARWELL
21°C; approximately 30% of the initial body mass is added during this time (Glen-
cross et al., 2000).
4. JAPAN
In Japan, young of the year Pacific bluefin tuna, Thunnus orientalis, are col-
lected off of Shikoku and Kyushu islands by commercial fisherman trolling small-
feathered lures along the edge of the Kuroshio Current. The live tuna are held in
onboard tanks with running seawater and are then transported back to the tuna
farms where they are transferred to large rectangular pens, measuring 24 by 50 m
and 15 m deep. Each pen can hold up to 5000 individual small tunas and over time
these tuna are divided among other pens to accommodate for growth. They are fed
10% of their body weight per day over the course of three meals consisting of
locally caught baitfish. The mass of the newly collected tunas ranges from 220 to
300 g; at 1 year of age they have grown to 4-6 kg. The population of tunas in
each pen is reduced by splitting the number of tuna into other pens at intervals
timed to the growth of the tuna, thus reducing the stocking density of the original
pen. At this stage the food ration is lowered to approximately 5% of the estimated
total mass of tuna in the pen. They are harvested at age 3 with a mass of approxi-
mately 40 kg (Suwa, 1989).
5. MEXICO
The size of the Pacific bluefin tuna collected for farming in the eastern Pacific
ranges from 20 to 50 kg, and they are 2-4 years of age. They are caught from
June through September in the waters off of Mexico and California. Fish are
maintained in pens until late January or February in a coastal area of Baja Califor-
nia, Mexico. The pen nets are 45 m in diameter and 15 m deep, and are stocked
with up to 45 mt of bluefin per pen. Bluefin are fed once per day with sardines
and anchovy, with food totals estimated to equal 5% of the biomass of tuna in
each pen.
B. Captive Tuna Research Facilities
The open ocean, pelagic environment of most scombrid species has made it
challenging to conduct field research. Their high metabolic rates and specialized
swimming result in significant space requirements if held in captivity. The major
challenge is that tunas must swim continuously, which makes collecting and cap-
tive care difficult.
1. KEWALORESEARCHFACILITY
In 1958 the National Marine Fisheries Service built the first permanent tuna
research facility specifically designed for maintaining tunas in captivity at Kewalo
Basin, Honolulu, Hawaii. The researchers at Kewalo Basin in collaboration with
10. TUNAS lN CAPTIVITY 395
the local tuna fishers pioneered the techniques for collecting, transporting, and
keeping yellowfin tuna, Thunnus albacares, in captivity. The holding facility con-
sists of three 76,000-liter circular tanks, alarger 7.57,060-liter tankdesignedspecifi-
tally for tunas, and a number of smaller research tanks of various sizes. A high-ca-
pacity flow-through water system provides 3000 liters of oceanic-quality water per
minute for this facility (Brill, 1999). The Kewalo Research Facility has operated
continuously since its inception, and has supported physiological and behavioral
studies of visual acuity, sound sensitivity, olfaction, energetics, thermoregulation,
geomagnetic sensitivity, and spawning and rearing of tuna eggs. The species inves-
tigated include yellowfin tuna, skipjack tuna (Katsuwonuspelamis) and kawakawa
(Euthynnus afinis). The Kewalo Research Facility has earned a highly regarded
reputation for the wide spectrum of scientific investigation conducted over the last
40 years by an international group of scientists. A partial list of scientific publica-
tions is included in the NOAA Technical Memorandum, “The Kewalo Research
Facility-Leading the Way for More Than 40 Years” (Still, 1999).
2. ACHOTINESLABORATORY
In 1984, the Inter-American Tropical Tuna Commission (IATTC) opened
Achotines Laboratory in Panama. Early work focused on the techniques of collec-
tion, transfer, and maintenance of late larval and early juvenile scombrid species.
Continued research included early life history studies of local scombrid species,
including the black skipjack (Euthynnus lineatus). In 1993 a mutual agreement
between the IATTC, the Republic of Panama, and the Overseas Fisheries Coop-
eration Foundation of Japan led to the building of an enlarged rearing facility for
yellowfin tuna. The new facilities, completed in 1997, include four holding tanks,
the largest of which is 1,361,900 liters. Successful collection of brood stock and
subsequent captive spawning events for the yellowfn tuna have provided larval
tuna for studies on age, growth, and food selectivity (Anonymous, 1994, 1996).
Additional investigations include nutritional requirements and growth rates of the
captive brood stock maintained in seawater ranging from 21 to 29°C (Anony-
mous, 1997).
3. JAPAN
The earliest attempts to keep tunas in captivity for studying culture and rearing
techniques occurred in Japan at the Fisheries Institute, Kinki University (Harada
et al., 197 1, 1973a,b, 1980), and at the Marine Science Museum of Tokai Univer-
sity (Suzuki et al., 1972). Subsequent to these efforts, both Pacific bluefin tuna
(Thunnus orientalis) and yellowfin tuna have been collected and kept in float-
ing ocean pens for both research and commercial farming in various locations
throughout the southern islands of Japan.
Two major facilities of the Japan Sea-Farming Association (JASFA) are dedi-
cated to research on breeding and rearing of tunas; they are located in the southern
islands of Japan. Yaeyama Station on Ishigaki Island, Okinawa Prefecture, estab-

lished in 1985, primarily works with yellowfin tuna. Holding facilities at Yaeyama
Station for brood stock consist of a series of anchored floating pens differing in
size, with the largest being 20 m in diameter and 8 m deep. Potential brood stock
is collected as young of the year (375 g) and raised to sexual maturity. Longevity
up to 7 years of age (80-130 kg) has been obtained with successful spawning.
Observations on hatching rates, larval growth rates, and diet effects on survivor-
ship are the focus of research (Masuma, 1992, 1993).
The second research station is located in Amami O’Shima, Kagoshima Pre-
fecture, and is the newest facility within the association, having opened in 1995.
It is dedicated to research on the breeding of Pacific bluefin tuna. This facility is
unique and the only one of its kind in the world. Mature and adolescent bluefin
tuna are held in a 14-ha cove, which is closed off from the outer harbor with
double barrier nets. The average depth of the cove is 20 m. Outside of this em-
bayment there are two floating pens, 40 m diameter and 23 m deep, used for
holding brood stock tunas. Tunas ranging from 5 to 20 kg have been transported
to both facilities by boat, and larger 80-kg bluefin tuna were successfully trans-
ferred from a commercial farm to the JASFA Station at Amami O’Shima by tow-
pen. Breeding behavior was first observed in 1997, and fertilized eggs were col-
lected at that time. Rearing of eggs started in 1997 and has continued each
summer for the last 3 years. The size of the juveniles at the end of 3 months is
3 cm. Estimated size of the current brood stock is 250-350 kg; feeding is done
once a day with a diet consisting of squid and mackerel with added vitamins (Ma-
suma and Oka, 1996).
4. TUNARESEARCHANDCONSERVATIONCENTER,
The Tuna Research and Conservation Center (TRCC) opened in the fall of
1994 and is jointly operated by Stanford University’s Hopkins Marine Station
(HMS) and the Monterey Bay Aquarium (MBA). The TRCC maintains a re-
search population of tunas and is vital link to the successful display of tunas at the
MBA in the outer bay exhibit. The two facilities together (research and display)
are currently among the largest facilities maintaining captive tunas in land-based
tanks. Currently over 130 tunas (three species) are being maintained for both re-
search and exhibit purposes. Early research on the techniques of maintaining tunas
in captivity was conducted in the TRCC facility and it serves as the exploratory
research center for investigating how to keep new species for display. The TRCC
facility maintains yellowfin, T. albacares, skipjack, K. pelamis, and Pacific bluefin
tuna, T orientalis, as well as ectothermic scombrids such as bonito, Sarda chilien-
sis, and Pacific mackerel, Scomber japonicus. This provides a phylogenetically
broad range of scombrid fish for comparative physiological study (Altringham
and Block, 1997; Ellerby et al., 2000; Marcinek et al., 2001a). Populations are
10. TUNAS IN CAPTIVITY 397
maintained at both facilities (TRCC and MBA) with little mortality (<lo%) for
long durations (up to 7 years for yellowfin and 3 for Pacific bluefin tuna). Research
is focused on the physiology and husbandry of scombrids and the development of
electronic tagging technologies for wild pelagic species. Captive populations of
tuna have been instrumental to the development of a successful electronic tagging
program. Methodology for archival tag implantation surgery and pop-up satellite
(PSAT) tag attachment to living tuna was perfected under laboratory conditions
(Block et al., 1998a,b). Testing of the tags in a controlled environment allowed
observation of survivorship, tag placement, suture healing, and, for the PSAT tags,
release and transmission function.
The facility contains four holding tanks, each with its own life support system.
The volumes of the four holding tanks are one 327,000, two of 109,000, and one
of 20,000 liters. The life support systems provide seawater at rates of 4536, 15 12,
and 378 liter/mm. These flow rates are equivalent to a turnover rate (the time
required for one holding tank volume to pass through the water treatment system)
of one tank volume of water every 75 min for the three larger tanks and one every
60 min for the smallest tank. Tunas’ high oxygen demand and excretion rates
coupled with a semiclosed recirculation system necessitates a high turnover rate
of seawater. The system is semiclosed, with a minimum of 400 liter min-r of new
seawater added to make up for water losses associated with routine tank cleaning
and nitrite dilution. Each system is independent of the others, but can be cross-
connected in case of equipment failure. The system supplies seawater 100% satu-
rated with oxygen to each tank at a set temperature, and at pH values between 7.7
and 8.0. Return water to the system does not fall below 85% oxygen saturation.
Biological and mechanical filtration is accomplished through the use of hori-
zontal rapid sand filters. The filters were selected to meet specified surface areacri-
teria (Spotte, 1970; Wheaton, 1993), that is, flow not exceeding 6 liter min-’ cm-’
of filter bed surface area. At this flow rate, mechanical removal of particulate
matter is thought to be most efficient. The high oxygen demand of tuna was the
first consideration in the engineering design for the life support systems and is met
by passing all filtered return water through packed aeration towers (Hackney and
Colt, 1982). Seawater returning from the biological filters is sprayed into the top
of the aeration tower onto a bed of high-surface-area bio-rings. The flow of water
is spread over the medium and a thin film of water is created as it passes down
through the packed column. Diffusion of gasses at the water-air interface results
in water saturated with atmospheric gases including oxygen. The return water to
the holding tanks for tuna is brought back to 100% oxygen saturation levels in this
manner. Make-up water is suppbed to the TRCC from Monterey Bay Aquarium
at a maximum flow rate of 454 liter min-’ and is added to the top of each aeration
tower at flow rates proportional to tank volume and stocking density. This volume
of water allows for dilution and flushing of residual waste products from the in-
dividual holding tanks.
Aeration towers perform multiple functions beyond bringing the returning

water back to 100% oxygen saturation. Off-gassing of excess atmospheric nitro-
gen gas (N2) can help prevent introduction of gas bubble disease to the captive
fish populations (Anonymous, 1974a; Colt, 1986). Also, when modified with a
countercurrent airflow source, towers can aid in stripping off excess carbon diox-
ide, which is essential in semiclosed recirculation systems (Colt and Bouck,
1984). The current engineering solution is to incorporate a means of off-gassing
CO, from the water in the aeration tower by injecting air into the lower portion of
the tower with a blower. The air flows up through the media countercurrent to the
water flow and strips off dissolved carbon dioxide, returning the pH to normal
values. Air blowers with outputs of 23.7 and 67.8 m3 mm-* provide high-volume,
low-pressure air to the 2- and 2.5-m diameter aeration towers. The airflow/water
flow rate ratio through the aeration towers is 4.75 cubic meters of air per liter of
water per minute per square meter of surface area-these flow rates have proved
to be sufficient to maintain the desired pH levels of 7.7-8.0.
Foam fractionator towers remove dissolved organic compounds from the re-
turn seawater through the attraction that occurs between the electric charge on
the surface of small air bubbles and the bivalent charges associated with most
nitrogenous waste products. A mixture of water and air is induced through a
venturi into the bottom of the fractionator tower. The air-water mixture contacts
the incoming water as it passes from the top of the tower to the bottom drain.
This countercurrent system allows maximum mixing and contact between the air
bubble solution and the filtered incoming water. The resultant foam mixture of
water and organic molecules is carried to the top of the tower where it is accu-
mulated in an isolated section of the tower and subsequently washed into a waste
discharge line. Approximately 20% of the return water is passed through this treat-
ment process before being added to the aeration towers. This water treatment sys-
tem physically removes organic compounds and consequently lowers the filtrate
load on the biological filters. A schematic diagram of the TRCC life support sys-
tem is shown in Figure 1.
Each of the three large holding tanks is fitted with a pliable vinyl curtain that
extends around the inner circumference of the tank. The function of the curtain is
to soften any potential collisions of the tuna with the tank wall. The curtain ex-
tends from just below the water surface to a distance of 10 in. (25 cm) from the
tank bottom. This permits surface skimming of the water into the overflow boxes
and cleaning the bottom along the tank edge. Each curtain is marked with vertical
black lines running from top to bottom. The lines are spaced 25 cm apart and are
2.5 cm wide. The purpose of the striping is to give a visual reference to the tuna,
marking the perimeter of the tank. An additional feature on each of the tanks at
TRCC is a 0.5-cm square, knotless nylon netting jump screen designed to prevent
fish from jumping out the tanks. The knotless netting is less abrasive than knotted
netting, thus preventing skin and fin abrasions from jumping fish. The netting has
significantly reduced mortalities associated with fish exiting the tank.
Protein Aeration
Skimmer Tower
Filtered Seawater Supply 100 Ipm
n-
110,000 Liter Holding Tank
J i?!:“““’
I Sand Filter
1,230 Ipm To Drain
Fig. 1. Diagram of the operational facility designed specifically to keep captive tunas at the Tuna
Research and Conservation Center in Pacific Grove, California.
Lighting of the tanks is accomplished with fluorescent lights fitted with high-
frequency ballasts that eliminate the 60 Hz flicker associated with fluorescent
lighting. The lights are controlled with timers that turn the lights on and off se-
quentially. This allows for subtle changes at dawn and dusk in light intensity,
preventing startling the fish with a sudden change in light, which may cause wall
collisions and injury or mortality to the specimens. A low-wattage night-light is
fitted above each tank, allowing the tuna to navigate without colliding with the
tank walls. A battery-powered night-light is placed over each tank and automati-
cally turns on in the case of a power outage.
III. AQUARIUM DISPLAYS OF TUNAS

AND RELATED SPECIES
One of the earliest attempts at maintaining a species of the family Scombridae

in captivity occurred at Marineland of the Pacific where a display of eastern Pa-
cific bonito was established in 1966. Courtship displays and related behaviors on
these bonitos were reported by Magnuson and Prescott (1966). Currently seven
aquariums in the world are displaying tuna, six in Japan and one in the United
States. Most of these displays were designed specifically for keeping tuna on per-
manent display. Aquariums in Japan maintaining exhibits include Tokyo Sea Life
Park, Nagoya Port Aquarium, Kaiyukan Aquarium in Osaka, Aburatsubo Marine
Park, Kagoshima, and Aqua-Marine Fukushima.
Tokyo Sea Life Park Aquarium in Japan was the first aquarium to design and
build a permanent display for tunas with a water volume of 2,200,OOOliters. Col-
lecting and research on captive care of tunas started in 1987 and included five
species: bluefin, yellowfin, little tuna (Euthynnus u&is), skipjack, and Oriental
bonito (Sardu orientalis; Abe, 1993). The opening ceremonies were held in Oc-
tober 1989 and it has been a popular attraction. Nagoya Port Aquarium, opened
in October 1992, includes a special exhibit featuring the Kuroshio Current. This
is a 670,000-liter display of bluefin, yellowfin, little ttmny, and skipjack. These
two facilities maintain exhibits of scombrids only; the other facilities keep tunas
in mixed-species community displays. Kaiyukan (July 1990) displays tunas in
a 5,400,000-liter exhibit with a large collection of sharks, rays, and other fish
from the surrounding seas of Japan. Kagoshima City Aquarium (May 1997) fea-
tures a 1,500,000-liter exhibit of tunas along with other teleosts and elasmo-
branches.
In 1998 Aburatsubo Marine Park (1986) added Pacific bluefin tuna to their
ring tank, which is also a community of mixed species. The newest aquarium to
open is the Aqua-Marine Fukushima (July 2000), a public aquarium that fea-
tures a 2,050,000-liter tank that is divided into two sections, the Kuroshio Current
(warm water) and the Oyashio Current (cold water). The Kuroshio section dis-
plays yellowfin, bluefin, and skipjack tunas.
Monterey Bay Aquarium’s Outer Bay Waters exhibit opened in March 1996.
The exhibit’s central focus is a 3,780,000-liter open ocean tank. The species of
scombrids displayed currently include Pacific bluefin, yellowfin, two species of
skipjack tuna, and bonito. Other species of fish, sunfish (Mola mola), barracuda
(Sphyraena argentea), pilot fish (Naucrates ductor), soupfin shark (Galeorhinus
galeus), and pelagic rays (Dasyatis violacea) make up the community population
of this exhibit display. The life support system is designed to specifically meet the
rigorous demands of keeping large numbers of tunas in captivity. High water turn-
over through biological filtration, ozone treatment of the water, and carbon diox-
ide off-gassing for pH control provide oceanic water quality.
IV. METHODS OF COLLECTION AND CARE
A. Collection
Specimens for the TRCC and MBA are collected using various methods. For
yellowfin tuna, the commercial liftpole or jackpole is the method of choice if
school fish can be chummed to the boat. Live bait, either anchovies or sardines,
are chummed to attract the tuna to the stern of the boat. The jackpole, which is
3.0-3.5 m in length, is fitted with a 2.5- to 3.0-m length of heavy test monofila-
ment line terminating in a barbless lure called a squid. The squid can be with or
without feathers and is moved across the water to attract the fish. At the instant
the tuna bites the squid, the fish is lifted out of the water and guided onto a smooth
vinyl tarp that is suspended over one of the holding tanks. The bar-bless hook
comes out of the fish’s mouth as soon as the tension on the line is reduced. Each
fish is inspected for injuries before sliding the tuna off the tarp into one of the
holding wells (5.3-7.5 m3). For skipjack a similar technique is used with lighter-
weight fishing gear.
Bluefin tuna are more challenging to collect and require the use of standard
rod and reel sportfishing techniques using baited barbless hooks. Bluefin behavior
differs from yellowfin in that they rarely will bite on the liftpole lure, which ne-
cessitates using standard rod and reel sportfishing tackle. The heaviest tackle that
the tuna will bite on is used. Bluefin are caught on 20-kg line with 2/O to 5/O circle
hooks. The hooked fish is brought to a swim step at the stern of the boat as rapidly
as possible and is led by the fishing line into a seawater-filled vinyl sling (Fig-
ure 2). The sling with the fish is lifted up onto the deck of the boat and the tuna is
guided into one of the holding wells. The use of the water-filled sling is a critical
part of the collection. It is fabricated from a smooth-surface, pliable vinyl mate-
rial, with the length, width, and depth matching the size of tuna being collected.
The construction allows for water to be held in the sling; overflow holes adjust the
water level to just cover the fish. Velcro straps and drawstrings at either end of the
sling are used to pull the ends together, reducing the risk of the fish slipping out
of the stretcher. The tuna tend to remain calm as long as there is water covering
them inside the sling. Removal of the tuna from the sling is accomplished by
pushing the head end of the sling down into the water and at the same time pulling
the sling back and away from the fish (Figure 3).
Fig. 2. The use of vinyl slings to transport tunas in an envelope of water has proven extremely
successful.
Fig. 3. Top sequence shows release of tuna into the wells during capture and collection. Bottom
sequence shows release of tunas in a tank and the ease of movement of the fish without human inter-
action with the surface of the animal. The use of the sling prevents having to touch the tunas.
An increase in oxygen consumption occurs in newly caught specimens (Good-

ing et al., 1981). This is compensated for by adding oxygen to the water pump
discharge lines that supply seawater to the holding wells. The oxygen saturation
levels are maintained at a range of 130-150% saturation for 1 to 2 h after collec-
tion and then reduced to 110% saturation. Oxygen levels are monitored continu-
ously during the collection period and are controlled as necessary. The collected
tunas for the TRCC are brought to land and are off-loaded from the boat using the
vinyl slings. The water level in the wells is lowered, permitting individual capture
of fish by a person in the well using the vinyl stretcher. Each tuna is then lifted out
of the holding well and is either placed into a temporary holding tank located on
shore or transferred directly into a specially designed transport tank for truck
transfer to Monterey, California. The transport tank volume is 11,400 liters. The
maximum internal dimensions are 3.7 X 2.3 m and 1.7 m deep; the inside comers
and bottom edges are curved, creating a more suitable environment for the tunas.
The tank is equipped with a recirculating water system, 400 liter m-l, and in-
cludes a venturi injection system for adding oxygen. Internal spray bars add water
to the top of baffle boxes that aid in aeration and removal of carbon dioxide, one
of the most important aspects of transport. Temperature control is very important.
The initial starting temperature of the transport water is adjusted to accommodate
an elevation in temperature over time and to provide best water temperature for
each species. For bluefin tuna, a low transport temperature of 15” C, has proven to
be best. The lower temperature allows high levels of dissolved oxygen and also
theoretically lowers the metabolic rate. Yellowfin tuna have been transported at
higher temperatures, 17-18°C starting temperatures, to more closely match the
collecting location temperature and also the temperature of their final holding tank
at the TRCC. The fish density ranges from 5.0 to 10.0 kg mm3 and transportation
time to Monterey is approximately 10 h. Once at the TRCC, the fish are individu-
ally removed from the transport tank, tagged with a passive induced transponder
tag (PIT), and measured.
The use of PIT tags allows researchers to monitor and track individual fish
within the collection. Fork length measurements are used to accurately estimate
the total biomass of fish held in each tank (important for calculating feeding ra-
tions) based on established length and weight relationships. Subsequent measure-
ments of these fish over time allow captive growth rate determinations to be
made. These data are used to calculate a regression function for change in mass
over time. The resulting regression formula can then used to determine the aver-
age growth of fish held in each tank and changes in biomass within each tank
over time.
B. Captive Care of Tuna
The feeding regime of tunas is calculated according to the biomass of fishes.

The dietary goal is to have each hsh consume a specified amount of kilocalories
per kilogram body weight per day (kcal kg-’ day-‘). When maintaining a fish
population at a specified caloric allotment, proximate analysis of total calories and
percent content for both fat and protein of food items is necessary as food items’
caloric content changes with time and size (Table I). If the food items are not
analyzed regularly, the caloric allotment given to the tank may be incorrect. From
these data, the amount of food to be fed to the collection can be calculated, and
the calories derived from fat can be monitored to achieve a diet low in fat. Food
items used for captive tuna consist of squids (Loligo opalescens and Illex sp.),
anchovy (Engraulis mordux), sardine (Sardinops sugax), smelt (Spirinchus
starksi), and a commercially available, high-vitamin-content gelatin mix. Feeding
observations of bluefin tuna have shown that they have a preference for sardines
and that initial feeding time of newly caught specimens can be shortened by of-
fering a diet mostly of sardines. For all species, having older specimens in the tank
that are eating helps start the feeding process.
The practice of reporting diet as a percentage of body weight can be mislead-
Table 1.
Proximate Analysis of Commonly Used Food Items for Tuna
Squid Sardines Herring Anchovy
Small Large Small Large Small Large Small Large

(28 8) (47 g) (35 8) (75 g) (11 g) (50 8) (11 8) (34 8)
Percent protein 16.6 16.5 19.0 17.2 14.4 16.5 16.2 16.3
Percent fat 0.6 0.6 2.1 15.3 4.2 9.6 0.9 12.9
KcalllOO g 63 66 97 208 96 153 73 182
ing as the caloric content of the food items can vary significantly between species,
size, and season. To avoid this problem, reporting diet as kcal kg-’ day-i takes
into account variations due to differences in caloric composition of the food and
facilitates applying a consistent feeding regime to the collection. These data
allow the recalculation of food rations to maintain a set diet of approximately
20 kcal kg-i day-’ for the yellowfin tuna. The bluefin tuna are fed a diet of ap-
proximately 30 kcal kg-’ day-i, based on the assumption that they have a higher
metabolic rate. Tuna are susceptible to the stress of overcrowding and poor water
quality. The effects of overcrowding may be expressed in various physiological
signs and in external physical appearance. Comparison of hematocrit values and
blood serum enzyme activity between wild caught and captive Pacific bluefin tuna
has shown a measurable decrease within 5 weeks of captivity; increases in fat
content in both the muscle and the liver were also noted (Murai et al., 1982).
C. Handling Techniques
It is often necessary to handle individual fish within the collection, which can
add stress to captivity. To reduce the chance of injury the following techniques
have proven successful. The water level is lowered to 85 -90 cm and a small group
of people enter the tank and, with a vinyl barrier net (crowder), isolate a section
of the tank. One end of the crowder is attached to the tank curtain and the crowder
is stretched across the tank floor, creating a section that can be closed off by taking
the free end of the crowder back to the tank wall. With the crowder in the open
position an individual fish is identified and guided into the closable section; once
the fish swims into this area the section is closed (Figure 4). The tuna can then be
guided into a stretcher for the purpose of moving to a new tank, physiological
monitoring such as blood sampling, or growth measurements.
D. Growth
Data on growth measurements of captive tunas reported in the scientific litera-

ture include larval culture work (Harada et al., 1973b, 1980; Harada, 1973; Olson
and Scholey, 1990), rearing of juvenile or young of the year tunas (Harada et al.,
197 I; Suzuki et al., 1972), and some reports of captive adults held for either brood
stock or commercial interests (Masuma and Oka, 1996; Carter et al., 1998). To
minimize compromising the health of the fish due to overhandling while recording
growth accurately in a captive population of fish, fork length measurements are
recorded at the time of capture and death. If possible, additional fork length mea-
surements are made when moving fish among tanks and during physiological re-
search activities (e.g., blood sampling) occurring in the tanks. This is a relatively
noninvasive technique for measuring growth as water can be kept in the sling,
0 0 000000
00 000000
,o 000000
0 000000
,oooooo
- 00 0 0 0
Fig. 4. To capture live tuna in the tanks, a crowder made of vinyl is used. The vinyl has numerous
small holes that permit the crowder to be moved through the water without much resistance. The fish
are cordoned off into one side of the tank prior to being captured with slings. The tunas are never
handled manually in any aspect of capture.
which greatly reduces struggling. Captive bluefin and yellowfin tunas have both
grown more slowly than their wild counterparts (Table II). Several factors may
affect growth in captivity, which may explain the differences between the wild and
captive populations of tuna. Wild tuna probably consume more food than captive
fish on a restricted diet, which is a likely explanation of the reduced captive
growth rates. Glencross et al. (2000) found that growth of farmed southern blue-
fin in sea pens in south Australia virtually ceased when the water temperature
dropped below 15°C. Captive yellowfin tuna are held at 20°C at TRCC, which is
at the lower end or below their thermal preference in the wild, 19 to 26°C (Carey
and Olson, 1982; Block et al., 1997; Holland et al., 1990). Temperature effects
probably play less of a role with captive bluefin as their growth rates are more
similar to the wild growth rate than the captive and wild yellowfin growth rates.
This is probably because the water temperature for the captive bluefin (18°C) is
their preferred temperature in the wild (Marcinek et cd., 2001b). Thus, the growth
of captive bluefin is probably more diet limited than temperature limited. Since
our captive yellowfin are at the lower end of their thermal tolerance, they are prob-
ably both diet limited and temperature limited.
Table 2.
Growth Rate of Bluefin and Yellowfin Tuna
Growth rate Growth rate

Bluefin tuna (mmday-l) Yellowfin tuna (mm day-‘)
Wild (Bayliff et al., 1991) 0.71 Wild (Anonymous, 1974b) 1.20

Wild (Bayliff, 1993) 0.68 Wild (Hennemuth, 1961) 1.18
Wild (Koski, 1967) 0.58 Wild (Davidoff, 1963) 1.11
Wild (Yukinawa and Yabata, 1967) 0.55 Wild (Wild, 1986) 1.07
Wild (Foreman, 1996) 0.52 Wild (Anonymous, 1983) 0.75
TRCC Tank 1 0.63 MBA Outer Bay Waters Tank 0.51
TRCC Tank 2 0.49 TRCC Tank 1 0.37
V. RESEARCH OPPORTUNITIES
WITH CAPTIVE TUNAS
Captive populations of tuna have been instrumental for physiological studies as

outlined above. Perhaps less appreciated is that they are also important for the cur-
rent rate of development and successof electronic tagging programs on tunas in the
wild (see Gunn and Block, this volume). The captive populations have proven ex-
tremely important for validating hypotheses from wild tagging data such as the na-
ture of the specific dynamic action or the warming of the tuna visceral region after
feeding (Figure 5). Controlled experiments with ambient temperature or caloric in-
take values that are regulated can be accomplished in a tank environment. This al-
lows for examination of tag data in relationship to known variables. Methodology
for archival tag implantation surgery and pop-up satellite tag attachment to living
tuna was perfected under laboratory conditions prior to moving to the wild (Block
et al., 1998a,b). Testing of the tags in a controlled environment allowedobservation
of survivorship, tag placement, suture healing, and, for the PSAT tags, release and
transmission function. Observations of archival tags in yellowfin tuna in captivity
have demonstrated that very small fish can handle the surgery quite well and show
minimal effect. In some cases fish are feeding the next day after archival tag implan-
tation (Block et al., 1998b). The ability to recover the tags from captive animals has
demonstrated that in all cases, internally placed tags are encased in a mesentery and
are almost always invested with tissues and blood vesselsupon recovery, indicative
of no rejection when placed in the peritoneal cavity.
External PSAT tag observations led to selecting a tag shape and a place of at-
tachment to the tuna that would minimize contact between the tag and the fish’s
body. Use of a controlled setting to examine dart head materials such as the perfor-
mance of nylon versus titanium has led the TRCC team to select the latter as the
optimal material for tagging. PSAT float development for both types of pop-up sat-
28.0
26.0
6e 24.0
I!!
2 22.0
[ 20.0
r-
18.0
16.0 1 I I I I I I
0 6 12 18 24 30
Elapsed Tfme (hrs)
Fig. 5. The warming of the stomach due to the specific dynamic action associated with digestion
in a captive Pacific bluefin tuna. This experiment documents the rise of body temperature (left arrow)
after ingestion of 1200 cal from an all-squid feeding. Right arrow indicates the bluefin regurgitating
the tag. The tank temperature remained constant at 20°C during this experiment. The electronic tag is
fed to the bluefin by insertion into the mantie of the squid offered as food.
ellite tags (Microwave Telemetry, Inc., and Wildlife Computers) was performed by
experimenting with the shape of the syntactic foam and examining the fish carry-
ing the tags in holding tanks. This empirical effort led to a float design that would
provide maximum buoyancy with minimal drag, further ensuring the success of
field applications. Long-term monitoring of the test fish and post-tag placement
for adverse effects on the tuna has led to a high return rate of the deployed tags.
The access to tunas reliably provided by penned wild fish also has benefited
the tagging programs as PSAT tags attached to Pacific bluefin tuna in pens located
in Baja California, Mexico, have provided further testing of the technology incor-
porated into these tags. These pens, 45 m in diameter and 15 m deep, presented a
more challenging physical environment for the testing. Greater space and deeper
water depths in the pens allowed for more active swimming behavior, further test-
ing tag attachment techniques and placement. Sea surface conditions at time of
tag release tested the transmission and flotation of the tags under natural condi-
tions. The characteristic dawn and dusk diving behavior associated with wild blue-
fin tunas wearing archival tags was observed in the tagged pen fish, indicative of
the isolume and not prey as the key motivation behind this behavior.
To further examine the use of the electronic tag technology on small Pacific
bluefin tuna prior to large-scale releases in the wild, a controlled set of releases of
captive bluefin from the TRCC facility have proven extremely useful for discern-
ing the efficacy of external tags on small bluefin. This provides a way to test
software as well as hardware on PSAT tags throughout the year. In November
1999 two small Pacific bluefin tuna were released from the TRCC into Monterey
Bay 0.4 km in front of Monterey Bay Aquarium (Figures 6 and 7). One fish’s tag
successfully popped up in this experiment and provided a test of new software
prior to a large-scale use of PSAT tags on wild bluefin tuna in the Atlantic. In
2000, several Pacific bluefin and yellowfin that had been in captivity from 1 to 3
years were released. Each bluefin was tagged with a PSAT tag programmed to pop
up in 5 to 60 days. The tags provided an opportunity to test a new leader and dart
system for small fish. These tunas were initially put into a tow-pen used for trans-
porting tunas to a commercial tuna farm. The release site was 10 km out of Mon-
terey Bay. The fish were released as a school, inclusive of individuals without tags
35N I
30N
Fig. 6. Release of a captive bluefin tuna with electronic tags allows testing of specific hardware,
software, tag applicator tips, and/or placement. In this experiment small Pacific bluefin tuna and a
single yellowfin tuna were released from the TRCC into Monterey Bay. Tag 99-473 (solid triangle)
was a 103-cm Pacific bluefin tuna that was tagged in November 1999 and carried a pop-up satellite
archival tag for a 5-day duration. All other fish (solid circles and solid square) were released from a
tow-pen simultaneously from Monterey Bay after over a year or more in captivity. These latter fish
were released on September 28,2000, and included tag 00-292 (solid circle), a 121-cm Pacific bluefin
tuna tagged for 45 days, and 00-288 (solid circle), a 117-cm Pacific bluefin tuna that carried a PSAT
tag for 60 days. Also released with a pop-up duration of 7 days was a 132-cm yellowfin (99-703, solid
square). The success of captive release experiments back into the wild helped to initiate studies on
wild populations of Pacific bluefin tuna.
4 Nov. 1999
90 ‘1 I I I ! 50
0:OO 6:00:00 9:00:00 12:OO:OO 15:OO:OO 18:OO:OO 21:00:00 0:OO:OO
Time
_--_-----l..----.--_- _.__ _ _"___ ------_.-~__~___ -.-______-__

17
7
16
15 /
!g 14
f 13
HE 12 .. . .. 8
!
E '1
I-" 10
81 i
0:OO:OO 3:00:00 6:00:00 9:00:00 12:OO:OO 15:OO:OO 18:OO:OO 21:00:00 0:OO:OO
Fig. 7. Top graph shows depth movements 2 days after release of Pacific bluefin W-473 in rela-
tionship to light. One day of the record is shown. Bottom graph shows water temperatures for the same
period. Fish were maintained at 18-20°C for a year prior to release. To date small Pacific bluefin
released from captivity have successfully carried the tags up to 4 months.
to increase their odds for survival in the wild. All tagged fish survived and their
pop-up tags released 0.3 -2 months after release. The captive yellowfin tuna PSAT
tag released on day 7 reported a position 224 km to the south of Monterey Bay. All
of the bluefin moved due south along the continental shelf of coastal California
(Figure 6).
VI. FUTURE EFFORTS
The current level of success at maintaining captive tunas for research and ex-
hibit has built upon the physiological knowledge of early researchers. Scombrids
present challenges unique and appropriate to their level of biological sophistica-
tion. The future will undoubtedly see an expansion in these efforts that reflects the
biological importance of what is perhaps the most highly evolved fish in the sea.
Numerous physiological, growth, and development projects will emerge from the
numerous facilities now keeping more diverse species spanning a larger range of
the tunas natural history. Several species have not been kept long term in any
facility (e.g., albacore and blackfin) and future efforts most likely will be focused
on the challenges of keeping these species in captivity. The new intensive efforts
to farm or ranch wild tunas will undoubtedly offer new opportunities for research.
New techniques for handling tunas in land-based tanks and penning facilities will
increasingly require novel techniques for transport, handling, and sedation. This
most likely will improve research opportunities for larger specimens. The combi-
nation of physiologists and aquarists working together offers unique solutions for
establishing the science and technology for maintaining, studying, and rearing
captive species.
ACKNOWLEDGMENTS
Gratitude and thanks are due to many people who have given assistance with this chapter and
with the maintenance of the TRCC facility. Without their support, guidance, and help this contribution
would not have been possible. Barbara Block is responsible for including this chapter and without her
continued contribution of support, guidance, and help with the writing, this effort would not have
occurred. I thank Don Stevens for his helpful comments on a draft of the manuscript. Andrew Seitz
and Tim Sippel, TRCC Research Technicians, contributed intellectually and in technical support.
Roger Phillips and Eric Kingsley, Applied Research Department, MBA, have contributed through their
efforts at providing water quality data necessary for the keeping of tunas in captivity and for Figure 1.
Special thanks are due to the Block Laboratory and to Paul Sund, who has provided excellent daily
care of the collection.
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Marcinek, D. J., Bonaventura, J., Wittenburg, J. B., and Block, B. A. (2OOla). Oxygen affmity and
ammo acid sequence of myoglobins from endothermic and exothermic fish. Am. J. Physiol. Re-
gular Integrative Comp. Physiol. 280, Rll23-R1133.
Marcinek, D. J., Blackwell, S., Dewar, H., Freund, E., Farwell, C., Seitz, A., and Block, B. A. (2OOlb).
Muscle temperature and behavior of Pacific bluefin measured with ultrasonic and pop-up satellite
transmitters. Mar. Biol. 138,869~885.
Masuma, S. (1992). Breeding of yellowtin at Yaeyama Station. In “Annual Report of Japan Sea-
Farming Association 1992,” pp. 53-56.
Masuma, S. (1993). Breeding of yellowfin at Yaeyama Station. In “Annual Report of Japan Sea-
Farming Association Annual (1993),” pp. 53-56.
Masuma, S., and Oka, M. (1996). Rearing of bluefin and yellowfin tuna in subtropical areas. Proceed-
ings of Fourth Jntemational Aquarium Congress Tokyo, Tokyo, Japan, Congress Central Office
of JAC ‘96.
Murai, T., Akiyama, T., Hirasawa, Y., Oshino, T., and Nose, T. (1982). Blood constituent levels and
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51-59.
Olson, R. J., and Scholey, V. P. (1990). Captive tunas in a tropical marine research station: Growth of
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6(2), 79-88.
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Wild, A. (1986). Growth of yellowfin tuna, Thunnus albucares, in the eastern Pacific Ocean based on
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naeus), in the North Pacific Ocean. Rep. Nankai Regional Fish. Res. Lab. 25, l-18.
11
TUNA CONSERVATION
CARL SAFINA
I. Introduction
II. Synopsis of Current Management Regimes
A. Atlantic Tuna Commission
B. Southern Bluefin Commission
C. Indian Ocean Tuna Commission
D. Inter-American Tropical Tuna Commission
E. Moving toward Management in the Central and Western Pacific Ocean
E Newly Emerging Global Standards
111. Major Tunas-Status and Trends
A. Skipjack
B. Yellowfin
C. Albacore
D. Bigeye Tuna
E. Bluefms
IV. Bycatch in Tuna Fisheries
A. Purse Seining Bycatch
B. Longline Bycatch
V. Southern and Atlantic Bluefin Tunas-Case Histories
A. Southern Bluefin
B. Atlantic Bluefin
VI. Summary, Conclusion, and Emerging Trends
In general, “conservation” is the struggle for long-term sustainability. Two

broad generalizations can be made about tuna conservation: (1) conservation
needs tend to vary inversely with species fecundity, and need increase with aver-
age size and the money paid for individual fish, and (2) conservation needs are
most serious in the Atlantic, followed by the Pacific and then Indian oceans, in
direct relation to the history and intensity of industrial-scale exploitation in each
ocean. The Atlantic foreshadows what might be expected in other oceans if the
Atlantic’s lessons go unheeded. Half the world’s tuna are taken from the central
and western Pacific, where no fully implemented international management re-
gime yet exists for waters of the high seas.
413
Tuna : Volume 19 Copyrtght 0 2031 by Academic Press
FISH PHYSIOLOGY All rtghts of reproduction m any form reserved.
414 CARL SAFINA
In terms of economic or political importance, the major tunas are the skipjack,
yellowfin, bigeye, albacore, and northern and southern bluefins. Skipjack account
for roughly half the annual world catch of these six tunas. Overexploitation of
skipjack seems to have been reached in specific areas of the Atlantic. Exploitation
of Pacific skipjack stocks appears low to moderate. Yellowfin landings appear
close to the maximum sustainable yield (MSY) level in the Atlantic, where fishing
effort and mortality may be in excess of levels associated with MSY. Pacific
yellowfin exploitation rates are considered moderate. In the eastern Pacific, recent
assessments suggest that increased effort directed at juvenile tunas is probably
reducing economic yield and sustainability for bigeye and yellowfin. Indian Ocean
yellowfin catches are increasing. Albacore are overfished in the North Atlantic,
and South Atlantic albacore are considered fully exploited. Albacore exploitation
in the central and western Pacific is relatively low and sustainable. Atlantic and
Pacific bigeye tuna populations have declined rapidly.
Bluefin tunas are everywhere depleted, and their recovery has not been al-
lowed anywhere. The case of the bluefin shows that when an animal is worth
enormous money, politics will go to great lengths to disfigure science.
I. INTRODUCTION
Virtually anyone who sees a living tuna is moved by the beauty of a life so
energized and yet so mysteriously cloaked by the sea. Tuna provoke an intensity
of interest that few other creatures engender. They have inspired Aristotle’s prose,
Salvador Dali’s painting, Pablo Neruda’s poetry, contemporary literature, inter-
national diplomacy, some of the highest prices paid for any creature, bitter policy
disputes, lawsuits, and fistfights. Not least, tuna have inspired science; their lives
remain largely unknown, beckoning our fascination. Unfortunately, study of these
superlative creatures for the sheer fascination of their exquisite beauty and ex-
treme biology is increasingly overshadowed by concern about their continued
existence in robust and viable populations. Can tunas bear the appetite of a world
with 6 billion people?
Perhaps a few words about the term “conservation” are in order. Conservation
can mean any of several things. Here I use it to refer to actions meant to prevent
long-term decline, to restore depleted populations, or to manage human activities
so as to achieve the sustainable use and continued robustness of natural popula-
tions. Conservation can take the form of a concept (ecosystem integrity), a policy
(sustainable yield, say, or recovery), or an action (not setting a purse seine around
small juvenile yellowfin tuna).
Two broad generalizations can be made about tuna conservation: In general,
conservation need is inversely related to species fecundity, and need increases
with average size and the money paid for individual fish. (This can also be viewed
with regard to the relative fecundity of tropical vs. temperate tunas. Tropical tunas
1 I. TUNA CONSERVATION 415
breed two-thirds of the year and may breed as early as age 2. This is distinct from
a southern bluefin that matures at age 12 and has a specil?cally restricted breeding
season and location.) Also in general, conservation needs are most immediate in
the Atlantic, followed by the Pacific and then Indian oceans, in direct relation to
the duration and intensity of industrial-scale exploitation in each ocean.
A third generalization is that, as for many fishes, much uncertainty exists
about population sizes, fishing mortality rates, natural mortality rates, and sustain-
able catch levels for tunas, and less is known of effective stock structure (i.e., not
just genetic stock structure, which can be homogenized by low levels of gene flow,
but behavior-actual movements, migration patterns, residence times, and aver-
age rates of mixing or behavioral separation of fish in populations). One reason
for biological uncertainties is that research funding has generally been dismal-
sometimes less than 1% of the value of the catch total (Anonymous, 1998b). Of
money that is spent on scientific activity, stock assessments often take nearly
all. A reasonable rule of thumb might be for agencies to spend on basic biology
%oth of the money spent on stock assessments.
In the next decade, new technology using electronic tags (e.g., Block et al.,
1998a,b; Gunn and Block, this volume) will provide new views and expanded data
frameworks for understanding the movements of fish and the distinctions between
populations in the sea.
Information about population trends, sustainable yields, and fishing mortality
is generally more developed in the Atlantic, followed by the Pacific and then In-
dian oceans-again in direct relation to the length of history of industrial-scale
exploitation and therefore the extent and history of efforts to establish monitoring
and management regimes in each ocean.
Therefore, information presented in this chapter will be most extensive for the
Atlantic, where a longer time series of information is available. As the world hu-
man population has grown and industrialized, humans have become essentially
one “stock” thanks to globalization of markets and the effects of modern transport
on the flow of genes and diseases. Consequently, the Atlantic’s tuna history is not
only a foreshadowing of what could happen in other oceans but a harbinger of the
political difficulties of bumping against biological limits in a world that refuses to
contain its technological, numerical, or economic growth.
We hear much about the increasing need to “feed the hungry from the seas.”
It may seem ironic that the less important a fish is as food for large numbers of
people, the more contentious its management. Tunas provide perhaps the best
example of this irony-particularly the highest-priced bluefin and adult bigeye,
whose depletion is almost entirely driven by the Japanese sashimi market. On the
world markets the bluefins (and to some extent bigeye tuna) are “boutique spe-
cies” commanding excessive prices among a few people with excessive appetites
for luxury and status-enhancing displays of wealth. For all the difficulty with man-
agement politics, in no sense can these fisheries be considered as producers of
Food for the Masses.
416 CARL SAFINA
In the case of the bluefin, particularly, we see the effects on nature, politics,
and science resulting from the tyranny greed imposes. In important local cases,
such as the east coast of the United States, recreational or sport fisheries targeting
juvenile bluefin (for charter boat sportfishing businesses or for private recreation
and home consumption) have evolved into politically organized alliances. Some
recreational sectors now exhibit a degree of shortsighted self-interest paralleling
the worst of the commercial fisheries, and with the same results: all user groups
exert political force to prevent tighter regulation of themselves, resulting in man-
agement’s failure to follow the best scientific information available (or even the
law), depleted populations prevented from recovering (from becoming more bio-
logically and economically productive), and scientific assessment processes at
times corrupted.
Ironically, catches from populations rebuilt to levels capable of supporting
maximum sustainable yield would in many cases be higher than current catches,
and are always higher than replacement yields from merely stabilized but depleted
populations.
So why is management of tunas worse for those species meaning less as food?
For other species-sharks, say-it is because they are deemed not worth enough
money to bother with. For bluefin and bigeye perhaps the same is true in a perverse
way: no one will starve if bluefin and bigeye go commercially extinct, and no
major economies will be seriously hurt. Those people benefiting from large profits
invest enough of their money into political influence to affect management deci-
sions. Not enough people care enough for recovery. There exists also an extreme
resistance by many fisheries management agencies-often led by Japan-to ac-
tively acknowledging the concerns of conservation organizations. Japan’s resis-
tance to conservation extends even to those few governments, like Australia and
New Zealand, who seek a more conservative approach to already-depleted re-
sources in need of rebuilding (United Nations, 2001a). In the United States, con-
servation groups are now accorded more room “at the table” than they were a few
years ago, but agencies usually yield more to user groups and demands of the
fishing sector.
Various tunas and tuna-like fishes (e.g., mackerels and wahoo) are caught in
world fisheries. In this chapter I will be focusing on the six most heavily exploited
larger tunas-northern and southern bluefin (Thunnus thynnus, Thunnus mac-
coyii), bigeye (Thunnus obesus), yellowfin (Thunnus albacares), albacore (Thun-
nus alalunga), and skipjack (Kutsuwonus pelamis)-rather than smaller, less
widely distributed, and less heavily targeted species such as frigate tuna (Auxis
thazard), bullet tuna (Auxis rochei), blackfin tuna (Thunnus atlanticus), or several
others.
Also outside the scope of this chapter is aquaculture. Breeding tunas for com-
mercial purposes, or growing wild-caught juveniles to more valuable market size
(“ranching”), has in recent years been attempted or is practiced in several parts of
the world, including Japan, Australia, Mexico, the United States, and the Mediter-
11. TUNA CONSERVATION 417
ranean. While these fish contribute to the market, their availability has not seemed
to alter the intensity of fishing for wild fish. Hence aquaculture has not really
matured in the mix of issues affecting conservation of wild tuna populations and
species, and will not be further explored here.
This chapter will briefly synopsize international management structures, syn-
opsize the status of the species, briefly discuss bycatch, delve a bit deeper into
case histories of the bluefins, summarize, and then consider the future.
II. SYNOPSIS OF CURRENT

MANAGEMENT REGIMES
The major international management regimes for tunas are the International
Commission for the Conservation of Atlantic Tunas (ICCAT), whose purview
covers the North and South Atlantic; the Inter-American Tropical Tuna Commis-
sion (IATTC), covering primarily the eastern tropical Pacific; the Commission for
the Conservation of Southern Bluefin Tuna (CCSBT); and the Indian Ocean Tuna
Commission (IOTC). These commissions are created by international treaties that
set the parameters for their functioning. Other international bodies such as the
Secretariat for the Pacific Community (formerly South Pacific Commission) and
Forum Fisheries Agency coordinate information exchange and accessagreements
in national waters of many Pacific Island nations but have no management man-
date. Beside international regimes, many countries have national laws governing
tuna fishing (at least on paper) in their Exclusive Economic Zones (EEZs), usually
within 200 miles of their shores. Some national entities cover immense geo-
graphic areas; for example, the Western Pacific Regional Fisheries Management
Council has jurisdiction of the U.S.-exclusive economic zone surrounding the
main Hawaiian Islands, most of the northwest Hawaiian chain, and waters sur-
rounding all U.S. possessions in the central and western Pacific. However, no in-
ternational management convention currently exists for the high seasregion of the
western and central Pacific, though an agreement is in development.
A. Atlantic Tuna Commission
The International Commission for the Conservation of Atlantic Tunas (ICCAT)

was created by treaty in 1966 and commissioned in 1969. Its founding was
prompted by rapidly expanding tuna fisheries in the eastern Atlantic and increas-
ing competition between purse seiners and longliners there, as well as by concern
about possible depletion of west Atlantic bluefin tuna. ICCAT assumed scientific
and management authority throughout the Atlantic and Mediterranean for “tunas
and tuna-like species.” In practice this has included both tunas and such taxo-
nomically more distant species as marlins (Istiophoridae) and swordfish (Xiphius
glad&)-in effect Atlantic tunas and billfishes.
418 CARL SAFINA
The commission is composed of roughly two dozen Atlantic-rim countries,

plus Japan (which is a major fisher, importer, and consumer of Atlantic tunas) and
China (on behalf of Taiwan). The commission’s scientific committee, the Standing
Committee on Research and Statistics, is composed of scientists from several
countries and compiles catch statistics and models population trends. The com-
mission’s managers-also organized by national delegations-are responsible for
setting fishing management policy, ostensibly based on scientific advice. The poli-
cies take the form of recommendations. Each country is then responsible for im-
plementation, monitoring, and enforcement. The effectiveness of implementation
and compliance thus varies.
The commission’s charter obliges it to coordinate research and management
so that Atlantic tunas and billfishes can be maintained at population levels that
permit the maximum sustainable catch (i.e., Bmsy,or the population or biomass
that will allow production of maximum sustainable yield). But the majority of the
fishes under ICCAT’s purview are overfished and/or depleted, including several
tunas, blue and white marlin, and swordfish. Berkeley (2001) provides a compre-
hensive review (see also bluefin case histories section later in this chapter).
B. Southern Bluefin Commission
The Commission for the Conservation of Southern Bluefin Tuna, or CCSBT,

was formed by Australia, New Zealand, and Japan in 1994, after a decade of in-
formal cooperation. This formalization was hastened into existence by increasing
fishing pressure by other countries and increasing scrutiny of the southern blue-
fin situation by environmental groups, who began discussing listing southern
bluefin under the Convention on International Trade in Endangered Species
(CITES) as a possible means of addressing ineffective management of southern
bluefin. CCSBT’s sole purpose is to manage fishing for southern bluefin tuna. In
the late 1990s serious disputes over sustainable catch levels occurred between
Japan and New Zealand/Australia (see bluefin case histories section later in this
chapter).
C. Indian Ocean Tuna Commission
The Indian Ocean catch of tunas increased in the 1990s from 18% of the world
total to 24%. In the late 1980s the Indian Ocean catch exceeded the Atlantic catch
by 20%; by the late 1990s it exceeded the Atlantic by 75%.
The Indian Ocean Tuna Commission (IOTC) grew out of a United Nations
(UN)-supported Indo-Pacific Tuna Development and Management Programme,
founded in 1982 (though it did not have a management mandate). IOTC, which
has a management mandate, was established in the late 1990s.
IOTC covers 16 species of “tuna-like” fishes (primarily tunas and billfishes).
Catches of these species have exceeded a million tons of reported catches (vessels
flagged for convenience usually do not report) since the early 1990s 85% of
which is tunas.
The Indian Ocean is unique in that artisanal fisheries take as much as industrial
fleets. Artisanal fisheries use gill nets, troll lines, and pole-and-line. The impor-
tance of artisanal fisheries has actually increased in recent years.
Longlining, which started in the Indian Ocean in 1952, had spread over the
entire Indian Ocean by the mid- 1970s. Longlines now take about a quarter of the
Indian Ocean catch. Their portion of the catch has the highest value, because they
take mostly large fish for Japan’s high-priced sashimi market. Purse seining, which
started in the early 1980s and now takes about 360,000 metric tons (mt), takes
smaller fish mostly for canning (IOTC, 2001).
D. Inter-American Tropical Tuna Commission
The Inter-American Tropical Tuna Commission (IATTC) was created in 1950

under a convention between the United States and Costa Rica. Present members
also include France, Japan, Nicaragua, Panama, Vanuatu, Mexico, and Venezuela.
Its original mission was to carry out research into effects of fisheries and natural
events on fish stocks in the eastern Pacific Ocean, and to make management rec-
ommendations. In the late 1970s IATTC became heavily involved in research on
the incidental mortality of dolphins in purse seine sets made on tunas associating
with dolphins. Currently IATTC has a tuna-billfish program to study dynamics
of these fishes and estimate the effects of fishing, and to recommend actions that
will keep populations high enough to allow maximum sustained catch. It also
has a tuna-dolphin program to monitor dolphin abundance and fishing-related
mortality, and to recommend practices minimizing fishing-related mortality to
dolphins.
In 1995, representatives of 12 governments, including most IATTC members
except Japan, signed the Panama Declaration. This declaration commits nations
to a legally binding Agreement to Conserve Dolphins, contingent on U.S. law
changing to reopen U.S. markets to tuna caught in purse seine sets made around
dolphins in accordance with the agreement (Allen, 2001).
Some observers believe the Panama Declaration has created an important op-
portunity for conserving the region’s Iish populations, reducing the bycatch asso-
ciated with its tuna fisheries, and building a transparent and participatory fisheries
management regime. In addition to containing measures designed to protect the
region’s dolphin populations, the declaration includes a number of key mandates
that build upon the conservation requirements of the UN Agreement on Straddling
Fish Stocks and Highly Migratory Fish Stocks. The declaration: (1) calls for the
adoption of management for tuna populations that will ensure levels capable of
producing maximum sustainable yield, based upon the best available science and
a precautionary methodology; (2) requires the establishment of measures that will
avoid, reduce, and minimize the bycatch of sea life; (3) mandates the adoption
420 CARL SAFTNA
of cooperative measures to ensure compliance with the declaration’s terms; and

(4) requires transparency in the declaration’s eventual implementation.
The only wrinkle is that dolphin populations are not recovering at the expected
rate. Some speculate that the stress involved in chasing them to exhaustion to get
a net around them causes miscarriages or separation and loss of small juvenile
dolphins (Hall, 1998). Consequently, animal defense groups have sued to block
efforts by the U.S. government to change the definition of “dolphin safe.” The
definition change would be necessary to implement the Panama Declaration and
again allow import into the U.S. of tuna caught by setting nets around dolphins.
E. Moving toward Management in the Central and

Western Pacific Ocean
The large pelagic fish populations of the Pacific Ocean are among the most
economically important in the world. Roughly half the world’s tuna comes from
the western and central Pacific region, which encompasses some 10 million square
miles of ocean. As the demand for these fish continues to escalate, concern for the
future of these populations is growing. Most are subject to little or no active man-
agement, and reliable information as to their status is largely sketchy.
Currently there is no fully implemented international management regime for
tuna or other large pelagic fisheries of the central and western Pacific. The Secre-
tariat of the Pacific Community (SPC; formerly the South Pacific Commission),
formed in 1947, is an international organization based in NoumCa, New Caledo-
nia. Its mission is to provide technical assistance to the Pacific Islands to improve
the economic and social welfare of the peoples of the South Pacific. Its 22 member
countries are spread across 30 million square kilometers from 130”E to 13O”W
and 25”N to 30”s (commonly termed the central and western tropical Pacific).
Over 98% of this area is ocean, much of which is within Exclusive Economic
Zones of members. SPC’s five main program areas are fisheries, health, commu-
nity education, agriculture, and socioeconomic statistical services-though fish-
eries is the largest program, and the oceanic portion of that program (as opposed
to coastal) is focused on tuna (Lewis, 2001).
The main role of the commission is statistical monitoring, biological research
(e.g., yellowfin age and growth, reproduction, tagging, stock structure, bycatch),
and stock assessment (Lewis, 2001). The SPC is not a management or conserva-
tion organization. Its geographic area, the western and central Pacific Ocean, has
no fully implemented international management body to deal with tuna fisheries
in the vast international waters of the high seas (Lewis, 1999). However, the re-
gion has very large tuna fisheries with a variety of different gears, local artisanal
and larger international fleets, and recreational fisheries.
Fisheries in the western and central Pacific have expanded rapidly. Catches of
roughly half a million tons in 1980 expanded throughout the 1980s as purse seine
fisheries developed, and purse seine catches peaked in 1998 at just under 1.2 mil-
lion mt. Regional catches totaled nearly 1.8 million mt in 1998, when western and
central Pacific catches represented 77% of the total Pacific Ocean tuna catch of
2.3 million mt, and 52% of the total 3.4 million mt world tuna catch (Hampton
et al, 1999).
By the end of the 1990s purse seines in the western and central Pacific caught
an estimated 860,000 mt, the pole-and-line catch took 240,000 mt, and the long-
line fishery caught 187,000 mt (Anonymous, 1998a). Domestic and artisanal fish-
eries took less than 10% of the catch. The catch was mostly skipjack (60-70% by
volume) and yellowfin (20-30%), with much lesser amounts of albacore (2-6%)
and bigeye (4-6%; Lewis, 1999).
From 1980 to the end of the 199Os, the purse seine fleet in the region went
from just 14 Japanese vessels to almost 200 boats, mainly from Japan, the United
States, Korea, Taiwan, and the Philippines (Anonymous, 1998a). Japan’s catch
shrank by more than half from 1980 to 1994 (Morishita, 2001) due to changing
patterns of effort. New fishing forces such as China and Indonesia are emerging
rapidly in the region. Further, the region is filled with diverse and often conflict-
ing commercial fisheries, subsistence fisheries, recreational fisheries, and environ-
mental conservation groups.
A complicated series of events has developed momentum in the region to
formalize and strengthen cooperative agreements aimed toward conservation. A
Multilateral High-Level Conference for the Management of Tunas was held in
December 1994, the first of several meetings to develop a body for conservation
and management of the tunas in the central and western Pacific region (Morishita,
2001). An Interim Scientific Committee for Tunas and Tuna-like Species in the
North Pacific Ocean (IX) was held in 1996 (Morishita, 2001). The ISC is con-
ceived as the scientific groundwork for a possible future management body (Mor-
ishita, 2001). Activities include establishment of swordfish, bigeye tuna, and
northern bluefin tuna working groups (Morishita, 2001). Eventually, management
will require development of stock-specific reference points against which stock
status can be measured. But current levels of funding for data collection, research,
and stock assessment of tuna fisheries of the western and central Pacific are
“insufficient . . . to allow fisheries to be guided by good science” and total less
than 1% of the value of the catch (about $1.7 billion annually; Anonymous,
1998b).
Countries of the western and central Pacific region, along with the United
States, Korea, Japan, China, and Taiwan, met in June 1997 in the Marshall Islands
to discuss the possibility of developing a management regime for the region’s
tunas and other highly migratory species based on the new UN treaty. The prime
motivation to develop a management regime stems from increasing fishing pres-
sure on yellowfin and bigeye tuna in the region as new vessels from China, Tai-
wan, and other nations have entered the fishery.
The parties agreed to a detailed negotiating schedule aimed at reaching final
agreement in three years. The parties issued a declaration of intent (the Majuro
422 CARL SAFINA
Declaration) that announced their commitment to undertake a number of crucial

activities, including applying the precautionary approach to the management of
large pelagics, collecting and sharing data in accordance with the UN Agreement
on Straddling Fish Stocks and Highly Migratory Fish Stocks, and cooperating in
monitoring, control, and surveillance of fishing activities.
The Majuro Declaration charted an ambitious agenda for conserving the pe-
lagic fisheries of the western and central Pacific through the development of a new
regional fisheries management organization. It represents a major breakthrough
and opportunity to establish a precedent-setting regional agreement for the con-
servation of pacific pelagics.
In June 1998, a third session of the Multilateral High-Level Conference met
and developed a revised draft for a convention on the conservation and manage-
ment of highly migratory fish stocks in the western and central Pacific. Many
laudable provisions were featured in “Article 5, Principles for Conservation and
Management.” This section states that contracting nations shall, among other
things, “protect biodiversity in the marine environment,” “apply the precaution-
ary approach,” “ assess the impacts of fishing, other human activities, and envi-
ronmental factors on target stocks and non-target species . . . and species associ-
ated with the target stocks, ” “take into account the interests of artisanal and
subsistence fishers,” and “adopt measures to ensure long-term sustainability.”
Though good language is just a starting point, these are reasons for optimism.
In September, 2000, the seventh session of the Multilateral High-Level Con-
ference adopted a Convention on the Conservation and Management of Highly
Migratory Fish Stocks in the Western and Central Pacific Ocean. Importantly and
unfortunately, Japan and Korea opposed, and China and two others abstained. The
convention has now been signed by 13 states, including the U.S., and Taiwan
(“Chinese Taipei”). This important convention, which covers all highly migratory
stocks in a vast ocean area where tunas are the primary commercial resource, is
the first to follow the format of the United Nations Agreement on Straddling Fish
Stocks and Highly Migratory Fish Stocks.
The implementation of this agreement in the next few years will govern the
management of half the world’s tuna, and roughly 10 million square miles of
ocean. The agreement will also establish an important precedent for the manage-
ment of other pelagic species in other parts of the Pacific and the world. The
fisheries of the western and central Pacific rest at a precarious moment in history.
In the coming decade we will either repeat the mistakes of the Atlantic or fashion
a regime that ensures the long-term sustainability of these important fishing ac-
tivities and the health of their associated ecosystems.
F. Newly Emerging Global Standards
The UN Convention on the Law of the Sea gives coastal states jurisdiction
over all resources, including living resources, in an Exclusive Economic Zone that
can extend up to 200 nautical miles from their coasts. Under the Law of the Sea,
the UN in 1995 concluded the Agreement for the Implementation of the Provi-
sions of the United Nations Convention on the Law of the Sea Relating to the
Conservation and Management of Straddling Fish Stocks and Highly Migratory
Fish Stocks. The UN states, “preservation and management of rapidly dwindling
fisheries resources are the underlying objectives of the Agreement” (United
Nations, 2OOlb).
Often referred to as the Agreement on the Conservation and Management of
Straddling and Highly Migratory Fish Stocks, this new global treaty is intended
to guide management of fishing for large pelagic species and other types of fish
that occur in international waters. This agreement will not enter into force until
the requisite number of nations officially ratify it (30 are required; at this writing
27 have ratified, and updates can be seen at www.un.org/depts/los/los164st.htm).
The agreement sets out acceptable standards and mechanisms for cooperation,
monitoring, control, and surveillance. The new UN treaty requires countries to
cooperate to manage these fish through methods aimed at preventing overfishing,
minimizing waste and bycatch, and conserving nontarget fish, marine birds, and
other marine wildlife. These conservation requirements apply both within and
outside of zones of national jurisdiction.
Importantly, the agreement embodies the precautionary approach (acting con-
servatively in the face of uncertainty to fulfill policy requirements and minimize
risk of damaging resource viability). This approach is now contained in various
international policy instruments. Support for the approach has grown, following
recognition that many world fisheries are depleted and that more cautious man-
agement could have prevented this. The agreement also states that management
must be based on the best available science.
The agreement attempts to achieve conservation objectives by establishing a
framework for cooperation. This includes international minimum standards for
conservation and management; and measures designed to ensure compliance and
enforcement on the high seas. It also requires countries to cooperate or join re-
gional fisheries management bodies. When the agreement is fully entered into
force, there will no longer the freedom to fish the high seas without obligation to
cooperate in management toward more sustainable fishing (Edwards, 2001).
III. MAJOR TUNAS-STATUS AND TRENDS
In terms of economic or political importance, the major tunas are the skipjack,
yellowfin, bigeye, albacore, and northern and southern bluefins. Longlines and
purse seines take most of the catch. Longlines take mostly larger adult yellowfin
as well as larger bigeye and bluefin (Anonymous, 1998a). Purse seine technology
and efficiency increased substantially during the 1980s and 199Os, with innova-
tions and advances such as bird-locating radar; omni-scan sonar; Doppler current
424 CARL SAFINA
meters; satellite-derived sea surface temperature information; radio buoys; net

depth recorders; deeper nets and more powerful winches, power blocks, and as-
sociated deck machinery; increased ability to store very large catches (up to
300 tons per set); and increased reliance on fish aggregating devices (FADS).
What purse seiners set the net around is the major determinant of fish size.
Setting around free-swimming schools, or dolphins, takes larger fish. Sets around
FADS, logs, or other floating objects catch considerable numbers of smaller fish,
notably younger yellowfin and bigeye (Itano, 1998; Miyabe and Takeuchi, 1998)
as well as high bycatch of many species. Most of the modifications to purse seine
technology in the western Pacific during the late 1980s and 1990s were designed
to increase ability to capture free schools feeding at the surface and unassociated
with objects or mammals, and to be able to quickly load and refrigerate large
catches (Itano, 1998).
In Garcia’s 1994 review of 20 stocks of bluefin, yellowfin, albacore, bigeye, and
skipjack, 14 were then overfished or depleted. Stocks believed not fully exploited at
that time were Atlantic albacore, western and central Pacific yellowfin, and skipjack
worldwide. This situation is somewhat changed. Fishing pressure for Atlantic skip-
jack appears now to be at or above maximum sustainable levels. Albacore are over-
fished and fully exploited in the North and South Atlantic, respectively. Increasing
effort directed at juvenile Pacific yellowfins appears problematic.
A. Skipjack
The skipjack is the most tropical of the tunas targeted by major fisheries, has
the highest metabolic requirements of all the tunas, and tends to remain shallower
than other tunas (Brill, 1994; ICCAT, 1998). They spawn year-round over vast
ocean areas in equatorial waters, and seasonally where the 24-26°C isotherm
extends (Anonymous, 1998a). They grow at variable rates depending on area,
maturing at about 42 - 45 cm in the Atlantic (ICCAT, 1998).
Worldwide, skipjack account for roughly half the annual catch of the major
commercially exploited tunas (skipjack, yellowfin, albacore, bigeye, and southern
and northern bluefin; IATTC, 1999a). Virtually all skipjack are taken by surface
gears (ICCAT, 1998).
Important changes in Atlantic skipjack fisheries in the early 1990s included
intensive use of artificial floating objects to concentrate fish, resulting in record
high catches. Atlantic effort has declined in terms of vessel capacity but increased
in terms of effective vessel effort, due to technology enhancements. No quantifi-
cation of effective effort exerted on Atlantic skipjack is currently available, though
it is known to have increased overall for the Atlantic (ICCAT, 1998).
In the Atlantic ICCAT has established eastern and western management units
due to lack of tram-Atlantic tag returns. ICCAT has no quantified estimates of
maximum sustainable yield, population size, or relative fishing mortality for At-
lantic skipjack tuna (ICCAT, 1998). No assessments of the west Atlantic stock
have ever been performed, and stock status relative to quantified MSY-based ref-
erence points is unknown (Mace, 1997). Catch per unit of effort seems to have
fluctuated without trend since the 198Os, suggesting that catches are sustainable
in the west Atlantic (Mace, 1997).
In the East Atlantic, purse seines take the majority of skipjack, followed
by baitboats. Most fishing is done by western European, north African, South
American, and Caribbean nations. Vanuatu also fishes the Atlantic for skipjack
(ICCAT, 1998).
ICCAT’s 1998 scientific committee reports that
there has been a declining catch in recent years, despite sustained fishing
effort and increases in efficiency associated with fishing objects. Most of
the catches have been made in a specific area, the equatorial area, where
remarkable decreases have been noted in the sizes and average weights of
the fish caught. These could be indications of a local over-exploitation
of skipjack. (p. 25)
ICCAT ( 1998) concluded, “in spite of the characteristics of this species, a

state of over-exploitation of skipjack seems to have been reached, at least in spe-
cific areas” of the Atlantic (mostly the tropical eastern Atlantic).
Skipjack have high fecundity, relatively rapid growth, and high natural mor-
tality at younger ages. Such a life history pattern is a powerful buffer against
high fishing mortality. That fishing power exerted on this species over such a
vast area of the Atlantic could apparently be enough to cause “remarkable de-
creases” in fish size says much about the ability of modern fleets to muster ocean-
transforming levels of pressure on various components of wild communities.
Skipjack constitute 66% of the western and central Pacific tuna catch (Hamp-
ton et al., 1999). From 1980 to the early 1990s skipjack catches there doubled,
and now total 1.8 million mt annually (purse seines take about two-thirds of this;
Anonymous, 1998a). Skipjack catch per unit of effort (CPUE) fluctuated at around
the same level from 1980 to the late 199Os, with an increase to an all-time high
in 1995 (Anonymous, 1998a). Technological advances and retirement of less
efficient vessels may have caused the increase in CPUE. Current catches are
thought to constitute a low to moderate exploitation level for western and central
Pacific skipjack. Skipjack are almost certainly not overfished in the eastern Pacific
(IATTC, 1999a).
B. Yellowfin
Yellowfin tuna is a cosmopolitan species of tropical and subtropical seas.Ju-

veniles form mixed schools with skipjack and juvenile bigeye tunas, and tend to
426 CARL SAFINA
remain in surface waters (ICCAT, 1998). Yellowfin can often be found deeper in
the water than skipjack.
There appear to be two Pacific stocks: eastern and west-central Pacific (Anony-
mous, 1998a). Exploited sizes run the range from small juveniles (30 cm) to adults
(e.g., 170 cm; ICCAT, 1998). They are caught trolling, on handlines, longlines,
and rod and reel, with purse seines, and by baitboats. Yellowfin compose roughly
35% of the world tuna catch (IATTC, 1999b).
In the Atlantic a single yellowfin stock is assumed due to rates of trans-
Atlantic tag recoveries. The main spawning zone in the Atlantic is the equatorial
Gulf of Guinea, and after spawning the fish are presumed to move west. Longline
catches show them distributed throughout the tropical Atlantic (ICCAT, 1998).
While Atlantic yellowfin recruitment has fluctuated without trend since the
1980s spawning biomass has generally declined (Figure 1). Fishing pressure
on juveniles increased significantly in the early 1990s when increased Atlantic
purse seining operations employing fish aggregating devices and targeting fish
associated with floating objects resulted in increased catches of juvenile yellow-
fin, juvenile bigeye, and skipjack. Atlantic yellowfin catches peaked in 1990 at
184,000 mt, and then declined 30% by 1997 (ICCAT, 1998).
Eighty percent of east Atlantic yellowfin catches are purse-seined, while in
the west Atlantic 40% is taken by purse seiners, 30% by longliners, and 15% by
baitboats. Longline effort increasingly targeting deep bluefin and bigeye tuna
has resulted in yellowfin being a smaller portion of the Atlantic longline catch
(ICCAT, 1998).
Reported Atlantic yellowfin landings appear close to the MSY level, and fish-
ing mortality may be in excess of levels associated with MSY (Figure 1). ICCAT’s
scientific committee said
it is important to ensure that effective effort does not increase further. . . .
Therefore the Committee reaffirms its previous recommendation that mea-
sures to reduce overall effort, or at least to freeze it at current levels, should
be initiated immediately. . . . The Committee also continues to recommend
that effective measures be found to reduce fishing mortality of small yel-
lowfin. (ICCAT, 1998, pp. 18-19)
There are insufficient data to fully evaluate the effects of a voluntary morato-
rium, begun in 1997, on fishing on floating objects. ICCAT (1998) continues to
recommend this and other measures to reduce effort on small fish.
In 1973, nearly 3 decades ago, the commission recommended a minimum size
of 3.2 kg, with a 15% tolerance for smaller fish in the catches. But overall per-
centages of undersized yellowfins are currently running about 60% for all gears in
the Atlantic, with baitboats catching 80% undersized fish. Most of these small fish
are caught in the east Atlantic where they school with, and are caught with, skip-
jack (ICCAT, 1998).
20
15
10
0
1950 1960 1970 1980 1990
2.0 Atlantic Yellowfin Spawning Biomass

lB
0.0 ! ,, I,. I,, l,, I ,, I ,,l,,,,,‘,,,1 I I I ,,I
1965 1970 1975 1980 1985 1990 1995

Year
Fig. 1. Trends in Atlantic yellowfin tuna landings (A) and spawning biomass (B). Y axis in B is
biomass relative to that required to support maximum sustainable yield. Data from ICCAT (1998).
428 CARL SAFINA
7 I I I I I I I1 1 I1 I I1 8 I I I I I
1975 1980 1985 1990 1995
Year
Fig. 2. Trend in catch per unit of effort for central Pacific yellowfin tuna. Y axis scale is relative
to base year 1976. Data from Anonymous (1998a).
Exploitation rates for Pacific yellowfin are considered moderate (Anonymous,

1998a). In the eastern Pacific, yellowfin tuna are the most important species taken
by purse seiners (IATTC, 1999b). Central Pacific yellowfin CPUE has fluctuated
greatly since the early 1980s (Figure 2), with no clear trend for purse seiners
(which catch mainly juveniles) or temperate-zone longliners (which catch mainly
adults), but with a declining trend for longliners in the tropical zone (Anonymous,
1998a).
Patterns of increasing fishing development in the western Pacific and Indian
Ocean are reflected in yellowfin catches (IATTC, 1999b). The approximate per-
centages of the world total yellowfin catch for different areas in the early 1970s
versus the early 1990s are as follows: eastern Pacific ocean, 45% versus 27%;
western Pacific, 25% versus 35%; Atlantic, 20% versus 12%; and Indian, 8% ver-
sus 26% (IATTC, 1999b).
In the eastern Pacific, yellowfin abundance underwent a sharp decline in the
early 1960s and 197Os, but recovered strongly in the 1980s and has remained
relatively high since. However, effort increased 27% in the last half of the 1990s
bringing effort to a level higher than necessary to take the maximum sustainable
yield (overcapitalization), and possibly enough to cause a population decline
(IATTC, 1999b). Further, increased effort directed at floating objects and fish not
associated with dolphins is taking smaller fish, “probably causing the sustainable
catch of yellowfin in the eastern Pacific Ocean to decline” (IATTC, 1999b).
IATTC now limits the catch of yellowfin tuna taken in the eastern Pacific Ocean
purse seine fishery to roughly 225,000 mt.
C. Albacore
The albacore is a widely distributed, mostly subtropical to temperate tuna.

Albacore tend to spawn in subtropical waters, though they do spawn in tropical
waters in some places. Albacore mature at about 5 years of age and 90 cm (fork
length) in the Atlantic, and somewhat smaller in the Mediterranean (ICCAT,
1998). Albacore are rather temperate in their distribution, and are considered to
constitute separate north and south stocks in both the Pacific and the Atlantic.
ICCAT also recognizes a Mediterranean stock.
Various fishing methods targeting albacore include trolling, baitboats, drift
nets, pelagic pair trawls, and longline. Other gears make minor catches. Juveniles
tend to remain shallower than adults (ICCAT, 1998). Consequently, juveniles tend
to be caught in surface gear, and adults tend to be caught more on longlines
(ICCAT, 1998).
The total Atlantic catch has declined following declining total effort since the
1960s (due to longlines shifting to more lucrative and deeper bigeye tuna), though
effort and catch in one component-the new surface fisheries-has increased
markedly since the late 1980s (ICCAT, 1998). Spain, Ireland, Portugal, France,
and the United Kingdom are among the more important fishing countries in the
North Atlantic, while South Africa, Namibia, Brazil, Taiwan, Japan, and Portugal
fish the South Atlantic. Boats from Italy and Greece, mainly, fish for albacore in
the Mediterranean (ICCAT, 1998).
For the North Atlantic, abundance of adult fish (age 5+) declined during the
late 1970s to mid-1980s, falling through the level needed to support MSY and
remaining there. Spawning biomass is currently only about half the level needed
to support MSY (Figure 3). Fishing mortality has generally been increasing re-
cently and now appears to be between 25 and 40% higher than that which would
generate MSY. ICCAT has highlighted the need to limit North Atlantic fishing
effort at current levels (ICCAT, 1998).
For the South Atlantic, abundance of adult fish declined markedly from the
mid- 1970s to the mid-1990s. Recent estimates suggest spawning stock and fishing
mortality variously above and below the level associated with MSY. These differ-
ences arise from revised catch data and trend changes in different indexes of abun-
dance. Considering these differing results and uncertainties, South Atlantic alba-
core are considered roughly fully exploited relative to MSY (ICCAT, 1998).
In 1998 ICCAT implemented a South Atlantic albacore catch limit of 22,000
mt, and most albacore-fishing countries implemented corresponding regulations
(this is designed to limit catches to 90% of the average annual catch between 1989
and 1993; ICCAT, 1998).
No ICCAT regulations exist for the Mediterranean (ICCAT, 1998). Mediter-
ranean catches are considered minor and no assessment has been done due to
insufficient information (Mace, 1997). In 1998 the European Union adopted a
regulation phasing out drift nets entirely by 2002 (ICCAT, 1998).
430 CARL SAFINA
O!,,,,,,,,,,,,,,,,,,,,,,,
1975 1978 1981 1984 1987 1990 1993 1996
Year
Fig. 3. Trend in spawning biomass (age 5+) for North Atlantic albacore. Horizontal line is
spawning biomass required to support maximum sustainable yield. Data from ICCAT (1998).
Pacific Albacore CPUE is relatively low or declining in many areas compared

with data from earlier years of the Pacific fishery, though recruitment seems rela-
tively stable and estimates of adult biomass seem strong (Anonymous, 1998a).
Though albacore are relatively slow growing and long lived compared to tropical
tunas, it is believed that the current exploitation rate in the central and western
Pacific is relatively low (probably less than lO%/year.) and sustainable (Anony-
mous, 1998a).
D. BIGEYE TUNA
Bigeye tolerate the lowest dissolved oxygen and water temperatures among
the major species in commerce (skipjack, yellowfin, albacore, and bigeye; Brill,
1994). Bigeye make extensive vertical movements and often feed deeper than
other tunas (ICCAT, 1998). The bigeye tuna is a generally understudied tuna de-
spite its increasing value and intensifying importance in tuna fisheries.
Bigeye mature at the beginning of their third year, at a fork length of about
100 cm (ICCAT, 1998). They spawn largely in tropical waters, and growth is
relatively rapid (ICCAT, 1998). Their Pacific stock structure is poorly known
(Anonymous, 1998a).
In the Atlantic, the Gulf of Guinea is a major nursery area. Young fish often
mix in shallow schools with yellowfin and skipjack tunas, often in association
with drifting objects or sea mounts. At larger sizes, bigeyes move into more tem-
perate waters and their proclivity for associations with other tunas and objects
diminishes (ICCAT, 1998).
ICCAT manages bigeye based on the assumption of a single Atlantic-wide

stock but notes the possibility of separate North and South Atlantic populations
(ICCAT, 1998). A recent genetic analysis of Pacific Ocean bigeye populations by
the Pelagic Fisheries Research Program (PFRP) was unable to detect major sub-
divisions (PFRP, 1998). Some bigeye move considerable distances, for example,
5% of bigeye tagged by the South Pacific Commission in the early 1990s moved
more than a thousand miles (PPRP, 1998). Yet bigeye also demonstrate consider-
able site fidelity-a considerable number of bigeye were captured at the release
site after more than 5 years at liberty (PPRP, 1998).
Bigeyes are killed primarily by longlines, baitboats, and purse seines. Long-
lines catch bigger fish (45-50 kg), baitboats take small to medium fish (20-
30 kg), and purse seines take small fish (5 kg; ICCAT, 1998).
In the Atlantic, most baitboats operate in the eastern North Atlantic, where
they take significant amounts of medium to large bigeye tuna; baitboats in other
oceans tend to take smaller fish. Japan and Taiwan operate enough longliners in
the Atlantic to take half the bigeye catch. Purse seiners targeting primarily yellow-
fins take significant numbers of bigeye tuna, again mostly in the eastern Atlan-
tic-primarily in the Gulf of Guinea nursery area-but also off Venezuela
(ICCAT, 1998).
For Atlantic bigeye tuna, fishing mortality rates have increased “sharply” since
the early 1990s for both juveniles and adults (ICCAT, 1998). ICCAT’s calculations
are that the Atlantic bigeye tuna spawning population has declined rapidly since
about 1993. In the mid- 1990s the Atlantic bigeye catch reached a record of 115,000
mt, declining to about 90,000 mt in the late 1990s. Increased use of drifting logs,
fish aggregation devices, and other floating objects, and technological advances in
sonar, deeper nets, and bird radar (for spotting feeding flocks), all helped increase
purse seine effectiveness and thus the catch of small fish through the mid- 1990s. De-
spite a minimum size regulation of 3.2 kg adopted in 1980, fully 70% of the fish
caught in 1996 were undersized. Apparent reduction of juvenile abundance led to a
voluntarily observed seasonal and area closure on FAD fishing in 1997, which con-
tinues today. The voluntary regulation has been deemed “very effective in reducing
fishing mortality for juvenile bigeye” (ICCAT, 1998).
ICCAT ( 1998) has calculated the maximum sustainable yield for Atlantic big-
eye at around 70,000 to 90,000 mt, but estimates that since 1993 (except in 1997)
the total catch of bigeye in the Atlantic has been near or over 100,000 mt, an
increase of 30,000 mt since the late 198Os/early 1990s due to increased fishing
effort by all three major gear types. According to ICCAT (1998, pp. 21-22; see
Figure 4)
The total [Atlantic] catch has been higher than the upper boundary of the
likely range of MSY since 1993, suggesting that the stock has declined
considerably. . . . The estimated current biomass is below Bmsy[biomass
required to support maximum sustainable yield] by 20-40%, and current
432 CARL SAFlNA
2 700 -A
% 600
2
2 500
t
$j 400
E”
.g 300
m
.if 200
3;i 100
0 I I I I,, ,,,,,,,,,,,,,,,
1975 1980 1985 1990 1995
r 0.6-
.E
s3 0.5 -
0.4 -
P
f.- 0.3 -
ii 0.2 -
0.1 -
04 ,,,,,,,,,,,,,,,,,,,‘I
1975 1980 1985 1990 199s
Fig. 4. (A) Atlantic bigeye tuna abundance estimates and (B) fishing mortality rates. Data from
ICCAT (1998).
F [fishing mortality rate] estimates surpass Fmsy[fishing mortality rate as-

sociated with MSY] by 50 to 120%. . . . The bigeye stock is already over-
exploited. In addition, current spawning stock biomass-per-recruit is lower
than 20% of its maximum, which corresponds to a threshold at which re-
cruitment overfishing may occur. . . . [Ylields would be expected to decline
in the near future to levels below MSY. . . . Although MSY levels are not
well determined, the recent high catch surpasses estimates from all models
considered. It is highly likely that this catch level cannot be sustained in
the long term and may result in substantial declines in stock size [in the
Atlantic].
Eastern Pacific bigeye longlining began in the 1950s (IATTC, 1999c), and
until the 1990s Pacific bigeye were caught mainly by this gear (IATTC, 1999b).
During the 199Os, sharply increased catches of bigeye resulted from increasing
use of fish aggregating devices by purse seiners (IATTC, 1999~). Pacific bigeye
have been subject to large and increasing surface catches of small and medium
fish during the late 1990s (Anonymous, 1998b). Five to 10% of purse-seined Pa-
cific “yellowfins” are misidentified bigeyes, and purse-seined bigeye catches have
increased sharply along with the sharp increase in fleet capacity (Anonymous,
1998a). Purse seine catches of bigeye in the eastern tropical Pacific are estimated
to have grown from 5000 mt in 1992 to over 50,000 mt in 1997 (PFRP, 1998).
CPUE for bigeye in the eastern tropical Pacific has declined to low levels in recent
years (PFRP, 1998). In 1999 IATTC passed a resolution to limit the catch of big-
eye tuna taken in the eastern Pacific Ocean purse seine fishery to 40,000 mt. When
this limit is reached, purse seine sets on floating objects are prohibited.
Declines similar to those noted in the eastern Pacific are not yet detectable in
the western Pacific, but such declines are expected as the level of juvenile catches
of bigeye by surface fisheries increases (FFRP, 1998).
Total bigeye catch in the eastern Pacific doubled between the early 1970s and
late 1990s and “the productivity of the stock has almost certainly changed due to
the increased exploitation of younger fish” (IATTC, 1999~). Biomass of bigeye
in the eastern Pacific generally declined during the 1990s (IATTC, 1999~).
Overall, Pacific bigeye numbers have declined significantly (Anonymous,
1998a; see Figures 5 and 6). Recent catches-about 150,000 mt per year Pacific-
wide (IATTC, 1997)~are approximately at or above the maximum sustainable
yield (Anonymous, 1998a). However, deficiencies in knowledge about bigeye
stock structure hinder conclusions about stock status relative to overfishing refer-
ence points (Anonymous, 1998a).
E. Bluefins
Taxonomy recognizes three bluefin tuna species. The southern bluefin ranges
from waters off New Zealand and Australia throughout the Indian Ocean and into
the South Atlantic. The northern bluefin ranges primarily throughout the North
Pacific and North Atlantic, mainly in temperate and subtropical waters. Atlantic
and Pacific northern bluefin are genetically dissimilar enough to be considered
separate species Thunnus thynnw and Thunnus orientalis (Collette, 1999).
Bluefins are by far the largest tunas, reaching 650 kg, and living upward of
20 years. They are characterized by late maturation, slow growth, cool-water life
histories, and long generation times. Atlantic bluefin spawn from mid-April to
June in the Gulf of Mexico and Florida Straits, and late May to July in the Medi-
terranean (ICCAT, 1998). Bluefin make some of the most extensive migrations of
any fish; their physiological adaptations allow exploitation of environments rang-
ing from subtropical spawning areas to subarctic feeding zones.
434 CARL SAFINA
3.0 -
2.5 -
; 2.0-
+
8 1.5-
0:
s l.O-
9
0.5 -
0.0~,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,‘,,,,,,,,,,
1950 1955 1960 1%5 1970 1975 1980 1985 1990
Year
Fig. 5. Relative abundance index estimates for Pacific bigeye tuna. Data from Anonymous
(1998a).
Southern bluefins and Pacific northern bluefins are taken mostly by longline.
Atlantic northern bluefins are caught by longline, purse seine, handline, harpoon,
rod and reel, and trap.
Pacific northern bluefin tuna are known to breed (based on larval distribution)
only between the Philippines and southern Japan, and in the Sea of Japan. From
Eastern Pacific
1
Western Pacifi
0
1952 1959 1966 1973 1980 1987 1994
Year
Fig. 6. Relative catch per unit of effort for Pacific bigeye tuna. Data from Anonymous (1998a).
1 I. TUNA CONSERVATION 435
1952 1957 1962 1967 1972 1977 1982 1987 1992 1997
Fig. 7. Pacific catches of northern bluefin tuna. Data from IATTC (1999a)
those only known origins, they inhabit much of the temperate north Pacific, east
to North America. In the eastern Pacific Ocean nearly the entire catch of bluefin
tuna is made by purse seiners fishing not far offshore from California and Baja
California (IATTC, 1999a).
Catches of Pacific northern bluefin tuna were as high as 35,000 mt as early
as 1956, and as low as 9000 mt in 1990. But as recently as 1995 fluctuating
catches went as high as 24,000 mt (IATTC, 1999a). Though recruitment has been
judged not to have declined significantly, IATTC (1999a) states, “fishing has
greatly reduced the abundance of mature [northern] bluefin in the Pacific Ocean”
(Figure 7).
Southern bluefin tuna inhabit three oceans in the southern hemisphere. The
only known spawning ground is an area south of Java and northwest of Austra-
lia. Juveniles migrate along the Australian coast, extending their range as they
grow until they are distributed throughout the circumpolar South Pacific, Indian,
and South Atlantic oceans. They mature at about age 8. A significant number of
large fish are more than 25 years old-and the maximum known age is 42
(ICCAT, 1998).
IV. BYCATCH IN TUNA FISHERIES
While this chapter is about tuna conservation, tuna fisheries create collateral
conservation issues. One prefacing comment is needed: an information sheet put
out by the Oceanic Fisheries Program of the Secretariat of the Pacific Community
436 CARL SAFINA
notes that vessel logbooks in one of the area’s tuna fisheries put the bycatch at 9%
of the catch, while observers report 45%. Honesty in reporting and information
quality and reliability are important and contentious issues in themselves. Suffice
to say there is considerable misinformation-some of it intentional. The follow-
ing is a brief overview of some bycatch issues in tuna fisheries where data are
relatively reliable.
A. Purse Seining Bycatch
The most widely publicized tuna bycatch is the dolphins in the eastern tropical
Pacific purse seine fishery. This complicated topic has been reviewed in detail by
Hall (1998) and Gosliner (1999). Perhaps the best publicized bycatch issue in-
volved the estimated 400,000 dolphins that were caught annually while netting
yellowfin tuna in the eastern tropical Pacific. Over the three decades after the tuna
industry mechanized and went from pole-and-line fishing with large crews to
purse seine netting with small crews around 1960, the eastern spinner dolphin
(Srenellu longirostris) population fell 80%, and that of the offshore spotted dol-
phin (Srenellu attenuara) fell more than 50%. This led to the United States’
dolphin safe policy which began in 1990, banning imports of tuna caught by net-
ting around dolphins. The success of this in reducing direct kill of dolphins in the
nets has been excellent. Dolphin kills went from just under 100,000 in 1989 to
3000 in 1997 (Gosliner, 1999). To simplify a complicated story, let it suffice
to say that some netters shifted from netting around dolphin schools to netting
around logs and floating objects. Unfortunately, “dolphin safe” netting methods
are not tuna, billfish, turtle, or shark safe.
Netting around objects can entail hundreds of times the bycatch that netting
around dolphins does. Hall calculates that because many kinds of marine animals
congregate around drifting objects, including juvenile tunas, saving 1 dolphin was
traded off against approximately 16,000 discarded small tunas, 380 mahimahi
(Coryphaena hippurus), 190 wakmo (Acanthocybium solanderi), 20 sharks and
rays, 1200 trigger-fish and other small fishes, 1 marlin, and other animals.
The preseining pole-and-line fishery entailed essentially no significant by-
catch and did not catch dolphins. Going back to pole and line would entail hiring
back the numbers of people who were laid off when the fishery became mecha-
nized. Considering that regulations are always resisted by the fishing industry on
the grounds that they would hurt employment, it is interesting how eager boat
owners are to embrace any new technology that will allow them to reduce their
payroll. However, the reality is not that simple. Purse seining has greatly extended
the range of trips because there is no need to return to coastal waters to refresh
bait supplies, and in the past the fisheries had some difficulty sustaining bait fish-
ing (Hall, 1998). Many believe the sohrtion is to refocus purse seining on dolphin
schools where that is possible, using new techniques that greatly reduce dolphin
deaths. But as noted above, dolphin populations are not recovering at the expected
rate, leading to speculation that the stress involved in chasing them to exhaustion
in order to net them, to catch the associated tuna, causes separation and loss of
small juvenile dolphins, miscarriages, or other problems (Hall, 1998). A change
in the U.S. government’s definition of “dolphin safe” would be necessary to im-
plement the Panama Declaration (see Section ILD) and again allow import into
the United States of tuna caught by setting nets around dolphins. When the United
States has attempted to make that change, animal defense groups have taken the
definition of “dolphin safe” back to the courts and blocked the effort.
Purse seining in most other areas does not involve setting around dolphins
because the tuna-dolphin association is not cosmopohtan. But most purse seining
involves considerable bycatch of undersized tunas and other species. Bailey et al.
(1996) report that in the western Pacific, tuna purse seines catch up to 7% by-
catch, with the most common species being amberjack (Seti& rivoliurm),
mackerel scad (Decapterus macarelh), rainbow runner (E&at& bipinmdata),
drummer (Kyphosis cineruscens), mahimahi, and ocean triggerfish (Canthidermis
maculatus).
B. Longline Bycatch
High seas longline fisheries for tunas and billfishes deploy some 750 million
hooks annually into the world’s oceans (Bonfil, 1994). The Atlantic, Indian, and
Pacific oceans have major tuna longhne fisheries targeting bluefin, yellowfin, big-
eye, and albacore tuna. Some of the fisheries, for example, the North Atlantic,
target mixed tunas and swordfish (Xiphias gladiw).
Longline tuna fisheries incur significant bycatch and discard of sharks and
other elasmobranchs, bony fishes, undersized target species, prohibited and pro-
tected species, and various mammals, birds, and turtles. Hoey (1995) examined
bycatch in western Atlantic pelagic long&e fisheries in five regions from the
Grand Banks to the Gulf of Mexico. D&aids ranged from 40 to 65% of the catch.
Of these, dead discards ranged between 15 and 35%. Discards included mahimahi,
lancetfish (Alepisaums sp.), oilfish (Ruvettus pretiosus), wahoo, various sharks,
undersized swordfish [about a quarter of all swordfish caught; National Marine
Fisheries Service (NMPS), 19993, and some birds, mammals, and turtles. Threat-
ened and endangered marine turtles are occasionally caught and most are released
alive, but they probably incur significant mortality from ingested hooks (estimated
at 30%; Aguilar et al., 1992). Twice as many turtles are caught when light sticks
are used (NMFS, 1997). NMFS (1997) has concluded that “sea turtle takes are
documented everywhere the fishery occurs.”
The Hawaiian longline fishery has significant interactions with marine turtles
(NMFWSWFSC, 1997). NMPS determined that Hawaiian longline interactions
with sea turtles “adversely affects green, leatherback, loggerhead, olive ridley and
438 CARL SAFINA
hawksbill turtles” and found that these species may not be able to sustain the
current level of estimated take on a continuing basis (NOAA, 1994). Rapid expan-
sion of the Hawaiian longline fleet from 37 vessels in 1982 to 166 in 1992 led to
interactions with endangered monk seals (Mona&us schauinslandi). As a result,
a 50-NM (nautical mile) no-longlining zone was created around the northwest
Hawaiian Islands (NMFSISWFSC, 19%). Small cetaceans reportedly occasion-
ally take bait or catch, and rumors of shooting seem plausible.
Hawaii has also seen skyrocketing retention of fins of sharks caught inciden-
tally to tuna fishing (i.e., sharks that were once released are now killed, and most
carcasses are discarded). Numbers of sharks “kept” rose from an estimated 2300
in 1991 to 61,000 in 1998, as retention went from 3 to 61% (Camhi, 1999). Bonfil
(1994) estimated the total high seas longline bycatch of sharks at 8.3 million ani-
mals annualIy, almost a third of the world catch of elasmobranchs reported by the
UN Food and Agriculture Organization (FAO) in 1991. Of the total, he estimated
over 4 million were blue sharks. Most sharks caught by tuna boats in most of the
world are killed for their fins. Estimates for shark bycatch total numbers in tuna
fisheries are very poor for most regions (Bonfil, 1994).
Bailey et al. (1996) also note that western Pacific longline bycatch data are
very poor, but report that over 50 fish, including 21 species of sharks, 7 species of
nontarget scombrids, 6 species of billfishes, and 21 other fishes, have been re-
ported. The shark catch often equals the tuna catch, and most are blue sharks
(Prionace glauca).
Many thousands of seabirds are killed annually in southern hemisphere long-
line fisheries. Sixteen species of seabirds were recorded taken in the Australian
Fishery Zone between 1988 and 1995. Many of these were albatrosses. Other bird
species reported killed on longlines are petrels, skuas, gulls, kittiwakes, fulmars,
shear-waters,and penguins (Ornithological Council, 1997). In some cases, catches
of shearwaters and petrels considerably exceed albatross catches. But it is only for
albatrosses, with their extremely low reproductive potential, that longline bykill is
known to be driving population declines. The Japanese southern bluefin tuna
fleet alone was estimated in 1990 to be killing 44,000 albatrosses annually
(Brothers, 1991).
Most longline fishing occurs on the high seas, and several nations longline in
the Southern Ocean with no regulations or reporting requirements (Hayes, 1997).
There are no data for seabird catch from the tuna longline fleets of Taiwan, China,
Korea, and others (E&e and McKay, 1997).
In the wandering albatross (Diomedea exulans), adult females’ foraging be-
havior brings them into contact with the southern bluefin tuna longline fishery
more than does males’ (Weimerskirch and Jouventin, 1987). In 1995 Australia
declared longline bycatch a “key threatening process” to seabirds under its En-
dangered Species Protection Act of 1992. The Macquarie Island subspecies of
wandering albatross was listed as endangered in 1995. The wandering albatross is
listed on the World Conservation Union’s (IUCN) Red List as endangered, and the
gray-headed albatross as vulnerable. Gales (1993) called direct fishing mortality

“the most serious threat facing albatross populations.”
The southern bluefin tuna fishery alone may have accounted for South Geor-
gia’s annual mortality of 2-3% of adult wandering albatrosses and 14-16% of
South Georgia’s immatures between 1980 and 1986 (Croxall et al., 1990, Croxall
and Prince 1996). This is enough to account for observed declines. Longline fish-
ing is the only identified cause of decrease in these populations. Longline fishing
for southern bluefin tuna also affects survival of wandering albatrosses breeding
on the Crozet Islands in the southern Indian Ocean (Weimerskirch et aZ., 1997).
Pelagic as well as bottom longiine fisheries take birds. Longlining contributes to
and may drive observed declines in northern Pacific albatrosses (Flint, 1995).
The Convention for the Conservation of Southern Bluefin Tuna imposes no
gear regulations to mitigate bycatch, so increased quotas such as Japan has pro-
posed for that severely depleted population would also lead to increased seabird
bycatch (Earle and McKay, 1997). The CCSBT”s awareness of the albatross by-
catch problem is reflected in its creation of its Ecologically Related Species
Group, but so far seabirds have not been a decisive factor in decisions on catch
limits (Earle and McKay, 1997). Australia requires the use of a variety of bycatch
mitigation devices on Australian and Japanese vessels. Because albatrosses take
bait that might otherwise be eaten by a tuna worth thousands of dollars, the fishing
industry has some financial stake, though albatross mortality is calculated to cause
only a low percentage of income loss (1% of its catch, valued at $5 million per
year). Estimates of up to five baits lost per hooked bird suggest the reason why
boats have been willing to use streamer lines to frighten birds away, as well as
mechanical bait-throwing devices to remove slack from branch lines and speed
sinking. Hooking rates can be sharply lowered by using streamers to scare the
birds (and save baits). Japanese vessels using tori (bird) lines and setting at night
have catch rates less than 0.02 birds per thousand hooks (Hayes, 1997).
V. SOUTHERN AND ATLANTIC BLUEFIN TUNAS-

CASE HISTORIES
The bluefin tuna is emblematic for failure to find the political resolve to act
toward recovery of severely depleted fish despite having generally reliable scien-
tific information. Scientists will find much in these case histories to suggest why
it is important for them to maintain professional vigilance over management pro-
cessesthat claim to be science-based.
Bluefins’ life histories of late maturation (up to 12 years) and restricted spawn-
ing areas make them more vulnerable to overfishing and slower to recover from
population reductions than faster maturing and more widely spawning species.
Because the prices surrounding them mn so high, bluefins are depleted every-
where they swim.
440 CARL SAFINA
Management of bluefin has gotten more complicated than management of

probably any other species. Wherever fishing quotas for bluefins exist, the quota
has always been kept too high to allow recovery. The resulting management con-
troversies keep managers busy making more complex rules for marginally sustain-
able quotas. It is as though a pilot whose plane is losing altitude concentrated not
on trying to gain altitude but on flying more and more precisely closer and closer
to the ground. In some cases bluefin management has become absurdly compli-
cated, like the United States’ Atlantic size categories of small school, school, large
school, small medium, large medium, and giant, with different regulations on dif-
ferent days of the week and closings and reopenings at different (but unpredict-
able) times of the year as different quotas for different local areas fill for parts of
the season, and those areas are closed and then reopened.
These unnecessarily complex regulations result from one simple fact: catches
are too high. Bluefins everywhere are too desired to be allowed to thrive.
Southern bluefin and the Atlantic northern bluefin are the two cases that best
highlight the recalcitrance of countries that have conceptually good management
frameworks in place and painstakingly developed scientific information available.
But, because of political pressure to keep bluefin catches as high as possible in the
short term, the countries fail to use those frameworks for recovering depleted pop-
ulations or maximizing sustainable yields.
The following case histories are detailed because the arguments over scientific
information and use of science in management have long and welldeveloped his-
tories. They are instructive about the fate of scientific information in management
disputes.
Conservation biology is usually defined as “science in the service of conser-
vation” (Noss, 1993). That prompts the question, what is conservation? While
good conservation policies start with well-articulated goals and excellent scien-
tific information, conservation is not science alone. Conservation is mostly poli-
tics-politics in the service of living nature. Conservation policies are only as
good as the goals and the tools available. A goal like “sustainable use” cannot be
achieved without adequate scientific tools with which to design management. But
even perfect information will never find its way into management without a con-
stituency advocating use of high-quality science to guide human activities. The
efforts of that constituency.of science advocates constitute much of what can be
called conservation work. Usually, “conservation” becomes the struggle for long-
term sustainability-the struggle to infuse management with long-term versus
short-term thinking and interests.
What authorizes us to judge management? Management is inherently value-
free until performance standards are agreed upon. Just as science becomes “bad
science” if it fails to conform to agreed standards of objectivity and repeatability,
management becomes “bad management” if it fails to conform to legally agreed
performance standards (almost all of which are science-based) such as maximum
sustainable yield, recovery targets, biodiversity preservation, the precautionary

approach, or best science. “Sustainable use” and “use of best available science”
have emerged as the most widespread standards for natural resource exploitation.
These standards are explicitly stated in legal instruments such as national laws,
regional agreements, global treaties, and tuna management conventions.
In the world tuna fisheries, the bluefin tunas best illustrate this tension between
science, legal requirements, and commercial politics.
A. Southern Bluefin
Southern bluefin have been heavily exploited for nearly 5 decades, mainly by
commercial fleets from Japan and Australia (ICCAT, 1998). They are caught pri-
marily far offshore Australia, New Zealand, and South Africa. The catch peaked
back in 196 1, at 8 1,605 mt, with the Japanese longline fishery taking 78,000 mt
(96%; ICCAT, 1998). Thereafter, catch per unit of effort decreased during 2 de-
cades of intensifying effort (Bdwards, 2001). By 1980 the catch declined to
45,000 mt and there was already serious scientific concern over the status of the
population. Australian surface gear catches, which take younger fish than long-
lines, peaked in 1982 with 21,500 mt (Edwards, 2001).
Australia, New Zealand, and Japan have had a quota system since 1986. The
first annual quota was 38,650 mt, “too high and too late to avert further decline”
(Edwards, 2001)-the familiar pattern of unwillingness to apply enough restraint
to get ahead of the problem.
In 1994 Australia, New Zealand, and Japan entered into a treaty creating the
Commission for the Conservation of Southern Bluefin Tuna, or CCSBT. This for-
malization followed a decade of informal cooperation, and was finally hastened
into existence by a combination of increasing fishing pressure from other coun-
tries and increasing scrutiny by environmental groups who were discussing inter-
national action to ban international trade of the species.
The parental biomass is estimated at 5 to 8% of the virgin biomass (Edwards,
2001), and parental and younger age classes are facing increasing fishing pres-
sure-“cause for serious concern” (ICCAT, 1998). A strong year class in 1987
was fished hard rather than protected as a way of increasing parental biomass
(ICCAT, 1998). (Shepherding the last strong year class into adulthood to stimulate
more egg production was the linchpin of the recovery of U.S. east coast striped
bass, in my opinion the world’s most successful recovery yet of a depleted fish
due to strong management. Unfortunately, this simple principle is not universally
applied.)
The population seems to have stabilized at a low level recently, but catches by
other countries are showing “marked and continuous increase” (ICCAT, 1998).
No consensus exists on whether the population will further decline, remain stable,
or increase. The Australian government calculates only a 36% chance, under cur-
442 CARL SAFINA
rent quotas, of southern bluefin recovering in the next 25 years to levels capable
of supporting maximum sustainable yield.
Australia, Japan, and New Zealand take 11,750 mt under quotas (5265,6065,
and 420, respectively), but recent actual catches have totaled about 16,000 mt
(ICCAT, 1998) due to catches taken by countries not party to the CCSBT (e.g.,
Taiwan, Indonesia, and Korea reportedly take 1400,2200, and 1600 mt per year,
respectively). These countries have entered discussions about possibly joining the
CCSBT in the future. Their catches have been demoralizing to the CCSBT coun-
tries. Success in including all the fishing countries is seen by some as crucial to
the credibility and ability of CCSBT to manage.
Japan’s market drives the fishing (most commercial bluefin fishing is driven by
the Japan market), and so Japan could limit imports as a way of forcing other
nations to join and abide by CCSBT conservation measures.
Unfortunately, Japan does not itself appear to strongly support CCSBT con-
servation measures. Japan had proposed an increase in the total allowable catch
in 1995. After Australia and New Zealand would not agree to increase Japan’s
quota, Japan refused to agree to be limited by a total allowable catch quota (TAC)
in 1996. [Additionally, in 1996 New Zealand and Australia sought agreement on
actions that could be taken to, among other things, minimize mortality to alba-
trosses endangered in the southern bluefin fishery. Japan would not agree on a
course of action, saying further work was necessary (Edwards, 2001).] When no
agreement to an increased TAC was reached, Japan began in 1998 an “experimen-
tal fishing program” in which it reportedly caught additional “experimental”
catches of 1500 to 2000 mt in 1998 and 1999-more than 25% beyond its quota.
In 1999 Australia and New Zealand took Japan to an international tribunal in
Hamburg, Germany, under the UN Convention on the Law of the Sea, for fishing
over its quota. Japan stood accused of violations of the Convention for the Con-
servation of Southern Bluefin Tuna, and of the Law of the Sea. Japan insisted that
it’s 65-vessel “experimental” bluefin tuna fishing program, operating off Austra-
lia’s west coast, was not to be bound by its quota limit because it was “scientific.”
Australia and New Zealand charged the program was for commercial, rather than
scientific, purposes (Japan makes the same specious claim of “scientific” hunting
of Antarctic whales, and following that lead, ICCAT has long disingenuously re-
ferred to all the commercial and sport fishing for west Atlantic bluefin as being
done under its “scientific monitoring quota”). Obviously, Japan was using the
pretense of science simply to increase its quota of a commercially valuable fish.
The two plaintiff countries claimed increased fishing by Japan threatened “se-
rious or irreversible damage to the southern bluefin tuna population,” and they
sought a temporary injunction to halt Japan. Japan argued before the tribunal that
bluefin were increasing in Indian and Southern ocean waters, and their “experi-
mental” catch was sustainable.
The court agreed with Australia and New Zealand, ruling by 20 to 2 that Japan
11. TUNACONSERVATION 443
must consider any fish it catches as part of its quota (the 2 dissenting judges cited
technicalities, not the legal theory of the case). In addition, Japan may continue
an experimental fishing program only if the other two countries agree, according
to the court verdict (United Nations, 2OOla). Whether Japan will comply remains
to be seen.
The condition of the southern bluefin has attracted international criticism.
IUCN added the species to its Red List of Threatened Animals, and prior to the
tribunal decision, Australia itself had considered proposing listing it on the Con-
vention on International Trade in Endangered Species of Wild Flora and Fauna.
B . Atlantic Bluefin
The Atlantic bluefin’s uniquely lengthy management history constitutes another

case study of disparity between consistent scientific findings and consistently un-
responsive management (Mather, 1974; Safina, 1993,1997; Berkeley, 200 1).
Boats fish for Atlantic bluefin from the Gulf of Mexico to Newfoundland,
from the Canary Islands to waters south of Iceland, and throughout the Mediter-
ranean Sea (ICCAT, 1998). Formerly an active fishery existed in the North Sea.
ICCAT manages Atlantic bluefin tuna as two separate stocks-east and west At-
lantic-based on the existence of two widely separate spawning areas (Gulf of
Mexico and Mediterranean), different ages and sizes at maturity (younger in the
Mediterranean), tag returns showing only limited trams-Atlantic mixing (ICCAT,
1998) and absence in the Gulf of Mexico of fish of the sizes that breed in the
Mediterranean Sea (Nemerson et al., 2000).
1. STATUSINTHEEASTATLANTICANDMEDITERRANEAN
The east and west Atlantic fisheries differ in various ways. Catches in the east
Atlantic (which for this discussion includes the Mediterranean, where roughly
three-quarters of the catch is taken) are far less controlled than those in the west
Atlantic. Eastern markets for smaller fish are more diffuse, and the catch from the
eastern population is greater than an order of magnitude more than that from the
west-west Atlantic catches, including discards, have ranged during the late
1990s from 2200 to 3000 mt, while those in the east have exceeded 48,000 mt in
recent years (ICCAT, 1998). (The disparate catches supportable by the two areas
further suggest separate populations.) Catches have recently been near historic
highs at around 40,000 mt, but projections indicate that they must be cut to 25,000
mt merely to halt the decline (ICCAT, 1998).
For conservation and management in the east, one of the greatest difficulties
is monitoring-merely obtaining information from the various countries and
points of landings. Italy and Greece have both gained reputations for unrestrained
fishing and poor reporting.
A variety of fishing gears catch bluefin in the east Atlantic. Purse seining takes
444 CARL SAFINA
75% (by weight) of the eastern catch. Since the mid-1990s Japanese longliners
have been exploiting a new fishing area in the North Atlantic near 60” north lati-
tude and 20” west longitude (ICCAT, 1998). Beginning in 1994, ICCAT adopted
a regulation prohibiting large longliners from operating in the Mediterranean in
June and July, but “there have been many reported activities by many longliners
flying flags of convenience or without any country identification . . . during the
closure period” (ICCAT, 1998). ICCAT (1998) observes that “the high demand
for the Japanese market is without a doubt the reason” for longliners ignoring the
closure.
Small fish are under heavy pressure in the Mediterranean (Mace, 1997).
Seiners routinely target age 0 fish. Fish under the 6.4-kg minimum size constitute
40 to 60% of overall catches in the east Atlantic and Mediterranean (ICCAT,
1998). ICCAT (1998) reports that recent area closures have helped reduce the
percentage of undersized fish taken in the Mediterranean, but Raymakers and
Lynham (1999) contend that in Spanish landings half of the bluefin tuna from the
eastern Atlantic Ocean and over 80% of the bluefin from the Mediterranean Sea
are below ICCAT’s minimum size.
For the eastern Atlantic and Mediterranean, ICCAT (1998) noted “a strong
decline in number and biomass of older fish (spawning stock) since 1993. . . . The
current catch level is not sustainable. . . . The committee continues to be concerned
about the intensity of fishing pressure on small fish. . . . Additionally, recent abrupt
increase of catches of large fish is of grave concern” (pp. 35-36; Figure 8).
..,,I I1111 I1 I1 m,,,,,,,,,,
1970 1973 1976 1979 1982 1985 1988 1991 1994 1997
Year
Fig. 8. Population trend estimates for eastern Atlantic (including Mediterranean) bluefin tuna
(age 5+). Data from National Marine Fisheries Service.
In 1994 the commission recommended a 25% reduction in bluefin catches in

the East Atlantic and Mediterranean (ICCAT, 1998). The most recent catches are
3 to 8% higher than in 1994 (ICCAT, 1998).
Fishing mortality as of the mid-1990s was considered “far in excess” of fish-
ing mortality associated with maximum sustainable yield (Mace, 1997). Addition-
ally, the 1995 spawning biomass was estimated at only 19% of that corresponding
to Bmsy,the biomass needed to support maximum sustainable yield (Mace, 1997).
Thus the eastern Atlantic bluefin population is considered “severely overfished”
(Mace, 1997).
Maximum sustainable yield for eastern Atlantic bluefin is considered to be
about 40,000 mt, which is near recent landings (Mace, 1997). However, to rebuild
the spawning population within 20 years to levels that can support that catch long-
term, catches should be about 20,000 mt (Mace, 1997).
2. DEFICIENCIES AT ICCAT
The bluefin problem in the Atlantic results largely from ICCAT’s structure and
approach (though the recently formed CCSBT’s short history is in some ways
worse due to large catches by nonparty members and Japan’s noncompliance).
ICCAT’s stock assessments and scientific analyses are conducted by the Standing
Committee on Science and Statistics, which is composed of whomever the mem-
ber countries designate to be on their delegation. This committee makes recom-
mendations to ICCAT’s managers, who likewise represent the various member
countries in respective delegations. These managers make recommendations in-
tended to be policy, for implementation by member countries. Implementation of
these recommendations is essentially voluntary, and the quality of compliance and
enforcement varies among countries. Fishing by certain nonparty countries fur-
ther exacerbates problems.
ICCAT’s science has generally been of high quality over its history (with the
notable exception of its 1998 west Atlantic bluefin assessment, discussed later).
Its management, however, has often responded inadequately to the advice of its
scientists. Consequently, the commission has failed to prevent the depletion of
most species of tunas and billfishes under its purview.
Berkeley (2001, p.136) says of ICCAT, “although science is supposed to be
impartial and objective . . . even at the scientific level, national agendas and indus-
try objectives are paramount and . . . color the analyses and interpretation of the
results.” Scientific results are often reported equivocally and in unclear language,
reflecting a reluctance to restrict fishing. As situations worsen over years and so-
lutions require more decisive action, restrictions become more difficult. “If there
is insufficient support to implement management in the initial stages of stock de-
cline, when sacrifices are minimal, there will certainly be little support to do so if
substantive reductions in catch and effort are required. This is how the downward
spirals that are so evident began” (Berkeley, 2001).
446 CARL SAFINA
Is ICCAT a net benefit for Atlantic tunas and billfishes? That’s debatable.
Without ICCAT some species’ status might be even worse (Berkeley, 2001). But
it is also possible that some species might be better off without ICCAT. The fishing
industry in the United States succeeded in getting the U.S. Congress to adopt a
law preventing the United States from setting more restrictive quotas in its own
waters than the ones ICCAT gives the United States. In practice this has prevented
the country from setting more restrictive quotas for west Atlantic bluefin and
swordfish within the U.S. EEZ (which contains major breeding, nursery, migra-
tion, and foraging grounds for both species).
The fishing industry argues that these species compose one pan-Atlantic
“stock” and that unilateral management could not affect a species’ population
trajectory. Is this true? In the early 1970s the United States unilaterally banned
sale of swordfish because of mercury levels. ICCAT’s data indicated that Atlantic
swordfish population recovered almost to pre-longlining levels in only about
6 years, and declined again when the United States relaxed mercury standards and
the fishery reopened. This unintended experiment suggests potential efficacy of
unilateral management in at least some cases.
Denial and conflict avoidance are major characteristics of ICCAT’s political
atmosphere. As Berkeley (2001, p. 136) notes,
there is a tremendous inertia in the system. The status quo is always the
path of least resistance. . . . Considering the condition of the stocks under
its jurisdiction, it appears that ICCAT has lost sight of its original goal of
maintaining stocks at MSY and has instead focused on keeping the process
operating smoothly.
As with many management agencies, procedure becomes the chief product.
ICCAT activity increased in the 1990s. It established requirements that bluefin
in international trade be accompanied by a statistical document that travels with
each fish (allowing illegally caught fish to be better tracked) and enacted a system
for identifying countries fishing in contradiction of or outside of ICCAT recom-
mendations (and sanctioning several of them). Berkeley (2001) notes that ICCAT
accomplished little until it came under outside scrutiny, particularly by nongov-
ernmental organizations: “the most significant change in ICCAT has been brought
about by the involvement and oversight of conservation groups.” These changes
have been mostly too little and too late, however. [In the case of west Atlantic
bluefin, where the truly significant changes involved quota cuts, ICCAT has since
reversed itself. As the immediate threat of outside intervention from the Conven-
tion on International Trade in Endangered Species (CITES) has seemed to lessen
(see next section), ICCAT has put the quota essentially back up to where it was
during the 198Os.l
ICCAT’s charter requires management to maintain populations at levels ca-
pable of producing the “maximum sustainable catch,” but east and west Atlantic
bluefin, north and south Atlantic albacore, bigeye tuna, swordfish, blue marlin,
and white marlin all have fishing mortalities above MSY and biomass below that
needed to produce MSY. If one compares ICCAT’s performance with its charter,
it is clear that this commission has not been effective.
3. MANAGEMENT IN THE WESTERN ATLANTIC

West Atlantic bluefin is the most depleted species in ICCAT’s portfolio. West
Atlantic bluefins were fished intensively in the 1960s by purse seiners targeting
small fish for canneries. Obvious depletion-less than a decade after industrial-
ized commercial targeting-led to reduction in the east coast purse seine fleet
from more than 20 vessels to 5 (and led in part to the creation of ICCAT in the
late 1960s). West Atlantic bluefin catches averaged roughly 8000 mt during the
1960s and 5500 mt during the 1970s. During the 197Os, commercial targeting
switched to large fish for export. Effort intensified and longlining on the western
breeding ground increased, prompted by Japanese prices often averaging U.S.
$10,000, and as high as $30,000, per fish and more.
ICCAT managers long rejected their scientific committee’s advice to reduce
catches. In 1981 the Commission’s Standing Committee on Research and Statis-
tics concluded that the western Atlantic’s bluefin tuna population was depleted
and that catches “should be reduced to as near zero as feasible.” But the commis-
sion’s managers set a 1160-mt annual quota for 1982, ostensibly for “scientific
monitoring.” The next year, ICCAT doubled this “scientific” quota to 2660 mt
due to political pressure.
The first quota in 1982 brought mortality rates down considerably and might
have stemmed the population decline. Under the 1983 quota, however, the popu-
lation continued to drop. (The quota is shared by Canada, Japan, and the United
States, which gets the major share.)
Large fish were targeted for export and immature fish targeted by U.S. recrea-
tional boats (which catch about half the fish, by number). Throughout the 198Os,
lax U.S. government monitoring left catches untallied until the following year,
allowing extensive overruns in the recreational sector’s catch of juveniles.
The excessive quota, intensified effort, and poor monitoring and enforcement
caused another spike in fishing mortality in the late 1980s. Because the population
was rapidly shrinking and the quota -though higher than ICCAT’s scientists had
advised-was not, high fishing mortality continued. By 1990 the breeding popu-
lation was at an all-time low. The mainstream “environmental” community got
involved in Atlantic bluefin conservation in 1991, asking ICCAT to reduce the
quota to a level that would allow recovery, and asking the U.S. government to
tighten monitoring on recreational catches of juveniles, to avoid overruns. ICCAT
managers clung to the quota it had implemented in 1983, and the United States
was sluggish in responding to overruns in the juvenile allocation.
Consequently, the National Audubon Society petitioned the U.S. government
448 CARL SAFINA
to list west Atlantic bluefin tuna under the Convention on International Trade in
Endangered Species, on Appendix 1 (Safina, 1993). Such a listing would have
prohibited international trade in the species. Virtually the entire market for large
fish is in Japan. Without export to Japan, the price would collapse and far fewer
people would incur the expense of fishing.
Proposals to CITES can only formally be made by governments of party
nations. The United States declined to carry the proposal after the U.S. fishing
industry and their congressional representatives opposed the idea. The proposal
was then made by Sweden, which at one time had considerable bluefin landings
but whose fishery collapsed.
Sweden was pressured to withdraw the CITES proposal, but first extracted
nonbinding language that ICCAT would act on its scientific information and re-
duce the quota low enough to initiate recovery (Safina, 1997). Threat of listing
under CITES led ICCAT to implement a modest quota cut in 1992 (reduced from
2660 to 2394 mt).
With increased scrutiny and the threat of eventual CITES action usurping their
authority, ICCAT made several other improvements. ICCAT instituted a require-
ment for documentation to accompany each fish in international trade. This mim-
icked the requirement of a CITES Appendix 2 listing; ICCAT was trying to blunt
the argument that CITES would do needed things ICCAT was unwilling to do.
Such documentation made illegal export and import more difficult. Increased vis-
ibility also caused U.S. enforcement to improve significantly during the 1990s
with better monitoring and seasonal closures when the U.S. cap was reached. A
new prohibition on sale of most juvenile bluefins by recreational boats (requested
by several conservation and recreational fishing groups and fought by commercial
interests) made reductions of possession limits more feasible; consequently the
United States sharply reduced daily possession limits for juveniles.
Under continued threat of CITES action, ICCAT agreed in 1992 to cut the
west Atlantic bluefin quota to roughly half its long-standing 2660-mt quota, but
gave themselves another 2 years to phase it in, first reducing the quota in 1993 to
1995 mt.
The National Research Council (NRC) convened a team to review the bluefin
science. The NRC review highlighted gaps in relevant biological knowledge and
stimulated a new infusion of funding toward important basic research. The NRC
report (NRC, 1994) confirmed the history of depletion. It chose, however, to high-
light the fact that in the prior 5 years or so the population appeared to have stabi-
lized-albeit at or near all-time lows (Figure 9). That opinion was interpreted by
the industry and its political lobbyists as a finding of “no decline.” This led to
widespread misinterpretation (Sissenwine et al., 1998)~and allowed ICCAT to
rescind the 50% cut before implementing it.
After that, ICCAT increased the quota several times. By 1999 it was 2500 mt,
including discards. This is close to where it was from 1983 to 1992, when the
breeding population had initially been roughly twice as large.
1970 1973 1976 1979 1982 1985 1988 1991 1994 1997
Year
0.30
B
0.25
1
-
Q 0.20 -
s 0.15 -
P
z 0.10 -
G
0.05 -
o.oo! I I I I I I I, I,, I I I I I I I I I I I I I I I I I
1970 1973 1976 1979 1982 1985 1988 1991 1994 1997
Year
Fig. 9. (A) Population (age 8+) and (B) fishing mortality rate trend estimates for West Atlantic
bluefin tuna. Biomass in 1975 was long considered a proxy for the spawning biomass required to
support maximum sustainable yield. Data from ICCAT (1998).
Recent assessments estimate “spawning” (age 8 +) biomass at only 13 to 18%

of that considered the target to support MSY. Thus the western Atlantic bluefin
population is considered “severely overfished” (Mace, 1997).
To summarize, after falling steadily during the 1960s and into the 1970s west
Atlantic bluefin have been managed under a series of catch quotas since the early
1980s. Spawning biomass shrank roughly 85% between 1975 (the initial year for
450 CARLSAFINA
quantitative population estimates) and the late 199Os, with biomass of fish aged 8
and higher falling from an estimated 42,000 to 7,000 mt. Despite advice by IC-
CAT’s scientific committee for a quota “near zero” in the early 198Os,ICCAT has
kept quotas averaging roughly 2300 mt. Under these quotas, the spawning bio-
mass fell sharply and remains near all-time lows.
4. 1998: ONE REGIME SHIFTCLAIMED,

ANOTHERONEESTABLISHED
ICCAT’s science has generally been exemplary. Virtually all the conservation
groups’ positions on quotas have been based entirely on ICCAT’s own science.
And ICCAT’s internal dichotomy has often been characterized as “good science
and unresponsive management.” In 1998, events surrounding ICCAT’s bluefin
assessment changed that characterization, at least regarding bluefin, to “bad sci-
ence and bad management.”
The U.S. Sustainable Fisheries Act of 1996 requires the National Marine Fish-
eries Service to publish an annual list of overfished species. A recovery plan must
be developed for all species listed as overfished. West Atlantic bluefin are now
listed as “overfished.”
Thus in 1998 ICCAT was faced by the U.S. delegation with needing to de-
velop a recovery plan that would satisfy U.S. legal requirements.
By prior arrangement, ICCAT’s Standing Committee on Research and Statis-
tics had agreed to conduct its bluefin assessment using a Beverton-Holt model.
Beverton-Holt projections indicated that: (1) the current catch of 2500 mt could
not be sustained, (2) 2000 mt was likely sustainable, but to have a 90% chance of
maintaining the current population level the catch would have to be reduced to
1500 mt, (3) a 2000-mt annual catch would have about a 50% chance of leading
to a slight increase in breeding biomass (at the end of 20 years the spawning
population would be about 20% of its 1975 level-still quite overfished), and (4)
to recover the west Atlantic bluefin to the biomass associated with maximum sus-
tainable yield within 20 years (the goal required by ICCAT’s charter and the time-
table resulting from U.S. law), median trajectories indicated the need for reducing
the catch to about zero.
Faced with such a bleak assessment, a scientific and management cat-and-
mouse game ensued whereby the task became, essentially, “can we satisfy the
legal need for a ‘recovery plan’ without reducing fishing?”
Consequently, a scientist who works as consultant for the main industry lob-
bying association, and whose presence on the U.S. delegation has been arranged
by the commercial fishing industry, introduced a new model late in the assessment
workshop.
Any model predicting whether a population will increase or decline requires
estimates of the relationship between parental “stock” and reproductive success
or recruitment, and most such estimates are based on past observations of year
class strength and parental abundance (“stock/recruitment relationship”).
The stock/recruitment function used in the Beverton-Holt model indicated

higher chances of good recruitment when spawning biomass is higher. Such a
relationship is the general rule with fish. Myers and Barrowman (1996) studied
nearly 400 data sets from different species, asking a series of questions: (1) Are
the largest groups of young fish entering a fishery produced by the highest popu-
lations of spawners? (2) Are the smallest groups of young fish entering a fishery
produced by the lowest populations of spawners? (3) Are above-average groups
of young fish entering a fishery produced by above-average populations of spawn-
ers? Their findings were that “the answer to all three questions is almost always
‘yes.’ ” More to the point, such a relationship for bluefin has existed within IC-
CAT’s own bluefin data (Figure 10).
The model introduced by the industry-paid scientist was a so-called “Zline
model.” While the Beverton-Holt model is a well-known standard, the “Zline”
model is an ad hoc model that has apparently never been used outside of ICCAT,
nor has it been independently peer reviewed or published.
Actually the models are so similar that it might be difficult to conclude which
model might be superior. Given the same data input, they would likely produce
similar output. But they produced very different results when ICCAT used them
in 1998 for bluefin.
The disparity in output arose mainly from the omission of data. In running the
2-line model, the committee omitted data from the 1970s-when estimated breed-
ing biomass and recruitment were higher.
I I t
50 100 150 200
Spawners, Year X (thoueends)
Fig. 10. Relationship between estimated numbers of spawning-aged west Atlantic bluefin tuna
and year classes of 1-year-old recruits they produced. Estimated numbers of breeders in a given year
(year X) are plotted against estimated numbers of I-year-olds of tbe following year (year X+ I). Data
from ICCAT and National Marine Fisheries Service.
452 CARLSAFINA
All of the data (1970-1994) were used to estimate the stock/recruitment pa-
rameters employed in running the Beverton-Holt model, whereas only data from
198 1 to 1994 were used to estimate the stock/recruitment parameters employed in
running the a-line model. Essentially, for running the 2-line model they discarded
all the information showing that higher bluefin tuna breeding populations pro-
duced larger year classes of youngjish.
Thus, predictions of recruitment from the 2-line model’s results could not at-
tain levels as high as those estimated in the bluefin population’s actual history for
the 1970s. Consequently, estimates of biological reference points, such as MSY
or Bmyr must correspondingly be lower than those based on higher possible levels
of recruitment in the discarded data. So the 2-line model reached its conclusion
through the committee’s discarding parts of ICCAT’s data set that indicated higher
recruitment in years when parental abundance was much higher.
Because it assumes that recruitment is much less dependent on parental bio-
mass, the 2-line’s recovery goal is about half the breeding population recovery
goal level identified for the last 2 decades by ICCAT. The 2-line model’s results
predict that a catch of 2000-2500 mt-roughly the current catch-had about a
50% probability of reaching this new, halved Bmsyin 20 years. (The Beverton-
Holt run indicates a catch of about zero would be required to reach B,,, in
20 years.) The 2-line’s projected MSY is 2800 mt; in other words, we are already
near MSY (the Beverton-Holt run indicates MSY would be about 7700 mt, so we
have a long way to go to rebuild).
Thus output from the 2-line model suggests that at catches near current levels,
within 20 years there is only about a 50% chance of reaching a goal that is only
half the prior goal. The recovery goal is much lower because the 2-line model
output suggests that bluefin recruitment would not-cannot-increase with in-
creasing parental biomass. These conclusions resulted from discarding the parts
of the existing data set showing higher recruitment with higher parental biomass.
Proponents justified discarding almost half the data by claiming that a “regime
shift” in the Atlantic had lowered the ocean’s carrying capacity for bluefin. They
claimed as evidence the fact bluefin recruitment has been consistently poor in
recent years. Rather than concluding- based on the data set-that recent poor
recruitment may be related to the severely depleted parental biomass, they “as-
sumed” poor recruitment was occurring because the ocean must have changed,
and discarded a large part of the “old” data from back when the ocean must have
been different (as evidenced by better recruitment). They also ignored the fact that
virtually every other fish or bivalve in the North Atlantic for which fishing pres-
sure has been reduced by management has shown an almost immediate population
increase, including among others New England cod, haddock, Atlantic herring,
sea scallop, and Atlantic mackerel; mid-Atlantic striped bass, weakfish, sandbar
shark, and summer flounder; and king mackerel and redfish off the southeast
United States (herring and mackerel, key foods for bluefin, have recovered to very
high levels.)
Thus the marked difference in estimates of MSY and rebuilding resulted from
data input choices. There was no revision in the diagnosis that bluefin were se-
verely depleted. In 1998 ICCAT estimated spawning biomass at only around 15%
of the 1975 level (and bluefin were already heavily fished by the 1970s). ICCAT’s
1998 scientific report even noted continued high fishing mortality: “A regulatory
recommendation stating that contracting parties should limit the fishing mortality
to recent levels came into force in 1975. Catch reductions have not been sufficient
to reduce fishing mortality rates to comply with this regulation.” (p. 33) If ICCAT
had based its rebuilding plan on the same modeling choices it had followed con-
sistently prior to 1998, it would have had to mandate a significant catch reduction.
ICCAT chose the most risk-prone of all the assessments produced; even the
output they chose projects a 10% chance of extinction by 2012. It predicts less
than a 50% probability that the population will rebuild even to the much lower
new “target.” ICCAT chose not to use the Beverton-Holt results because they
indicated that Bmsywas higher, that recruitment was related to spawning popula-
tion, that the sustainable catch was much lower, and that rebuilding would require
very low catches in the near term.
The key point is that IC!CAT’s scientific committee confounded the question
of choice of model with the intentional omission of data. Thus many observers
have been under the impression that the choice of model, not the choice of data,
resulted in the disparity of results between the two models’ output. One wonders
whether the ad hoc 2-line model was introduced specifically so the report could
conclude that it had no basis for deciding which model was superior, to call at-
tention away from the fact that much of the data had been dumped to produce the
2-line model’s very different output. Inability to distinguish which model was su-
perior was how it was portrayed in the scientific committee’s report to the man-
agers, and that is the reason the managers gave for choosing the results produced
from the 2-line model.
By introducing and pressing use of the 2-line model and discarding the bluefin
data showing the positive stock/recruitment relationship, the industry had figured
out a way of corrupting the scientific process enough to construct a justification
for leaving the existing catch in place.
As a result of all the above, the committee’s 1998 report says, “to move with
about a 50% chance of reaching biomass levels supporting MSY [the 2-line’s new,
much lower MSY] within 20 years, current catches need not be reduced under the
2-line stock-recruitment relationship.” (p, 34)
Yet ICCAT’s management delegations voted to raise the quota slightly, to
2500 mt.
Thus, ICCAT’s “recovery” plan lowered the recovery goal by half, allowed
only a 50% probability of reaching this halved goal, and raised the quota slightly.
The 1998 quota returned catches to virtually the same levels that had been in place
during 1982-1992, when the population declined from a much higher level to
remain near all-time lows.
454 CARL SAFINA
In my opinion, data were omitted from the analysis to comply with an a priori
determination to develop a seemingly scientific way to avoid reduction of the
quota. The “assumption” that the higher recruitments of the 1970s are no longer
achievable (because of a “regime shift”) was not a scientific assumption as we
understand the term: a logical assumption based on the best objective considera-
tion of all relevant known factors. Rather, this “assumption” was merely an ex-
cuse because these “scientists” were working for the fishing industry to do every-
thing they could to keep catches high.
This was their best response to the question, “how can we come up with a
recovery plan without reducing fishing ?” Flimsy and transparent as this was, com-
plicity by other scientific representatives caused both by intense U.S. congres-
sional pressure and other nations’ proclivities allowed the scientific committee and
managers to claim that they had no basis for deciding which of the two models
yielded more realistic results.
The U.S. Magnuson-Stevens Fisheries Conservation and Management Act
(FCMA) mandates that within 1 year of a stock being listed as overfished, the
Secretary of Commerce is legally obligated to prepare “a fishery management
plan, plan amendment, or proposed regulations . . . to end overfishing . . . and to
rebuild the affected stocks” to population levels capable of producing “maximum
sustainable yield.” The peculiar 1998 bluefin plan slashes the recovery goal in
half, has a poor probability of reaching even the lowered goal, and raises the an-
nual catch. Contrary to U.S. law, the “recovery plan” fails to project rebuilding as
required and allows overfishing to continue. In fact, even if accepting the defini-
tion of overfishing derived from the 2-line model, the “recovery plan” allows a
fishing mortality rate higher than the one calculated as the threshold that consti-
tutes overfishingfir 1.5years offhe 26year recovery period. The “recovery plan”
thus appears illegal (Audubon v. Daley, 1999).
In every substantial way, this was a United States-driven plan. The scientific
results and report were driven by the industry’s hired consultant on the U.S. sci-
entific delegation, and the management position was driven or complied with by
commissioners representing U.S. fishing interests. The United States introduced
this plan and brokered its adoption. Japan was happy to avoid quota reductions
(and initially suggested an even higher quota). Canada initially pressed for real
rebuilding even though it would mean catch cuts, giving the United States another
opportunity to do the right thing. Canada capitulated to the U.S. position only later
in negotiations.
As a recovery plan it is at best a misnomer, because rather than claiming to
recover the west Atlantic bluefin, it claims first that the fish cannot recover due to
a regime shift, and then plans to “recover” them to a much lower target by increas-
ing the quota. In practical terms, it’s not possible. Even by its own calculation it
allows a fishing mortality rate in excess of its overfishing threshold for 15 years
out of the 20-year period. And quite simply, how can one expect recovery at the
same catch level that coincided with a major decline from a much larger popula-
tion level over 2 decades?
VI. SUMMARY, CONCLUSION,

AND EMERGING TRENDS
The status of tunas around the world is poorest in the Atlantic, better in the
Pacific, and perhaps better still, though least known, in the Indian Ocean. Fishing
pressure for Atlantic skipjack and yellowfin appears now to be at or above maxi-
mum sustainable levels. Albacore are overfished and fully exploited in the North
and South Atlantic, respectively. Atlantic bigeye have rapidly declined.
Pacific skipjack are under low to moderate levels of exploitation: yellowfin
stocks are under generally moderate exploitation pressure, though increasing ef-
fort directed at juvenile yellowfins and bigeye appears problematic. Albacore
exploitation appears low. As in the Atlantic, Pacific bigeye populations have de-
clined rapidly. Indian Ocean tuna fisheries and management and monitoring are
all at earlier stages of development, but fishing is increasing. Bluefin tunas are
everywhere depleted.
A striking aspect of this survey is that the sea is not so large, nor the human
population so small, to exempt even extremely fecund and very widely distributed
organisms such as skipjack and yellowfin tuna from concern about sustainability.
Fishing pressure is now developed enough to drive long-term declines even on the
scale of ocean basins. Just a few years ago it would have seemed highly unlikely
that even Atlantic skipjack and Pacific bigeye would suffer declines that appear
attributable to fishing.
Future recovery of depleted populations, and sustainable management of all,
will require much better commitment and better scientific understanding than have
been applied to tuna conservation and management until now. Scientific activity
is increasing and new technologies promise large advances in biological under-
standing in the near future. The challenge is particularly clear for the central and
western Pacific high seas and the Indian Ocean, where management regimes are
emerging. We must help ensure that these management regimes will learn from
and greatly improve upon, rather than repeat, the performance of ICCAT with
regard to Atlantic tunas and CCSBT with regard to southern bluefin. Recent signs
of increased responsibility and improved management by New Zealand, Australia,
and central Pacific countries are encouraging. Implementation of the 1995 UN
agreement on high seas and straddling stock fisheries would further help harmo-
nize and improve performance standards for management, conservation, and re-
covery of tuna populations.
Where else might the future take us? Up to now, fishery management, when
practiced, has been the near-exclusive domain of governmental agencies regulat-
456 CARL SAFINA
ing catches by tonnage and season. One large exception was the consumer move-
ment in the United States that brought its concern over dolphin deaths to the mar-
ketplace so forcefully that major tuna canners pledged that their products would
henceforth be “dolphin safe.” The consequent U.S. legislation prohibiting import
of tuna netted under dolphins merely followed where the marketplace had already
gone. New consumer education campaigns currently underway may widen the
role of consumer choice in fishery management, and management may become
increasingly company-driven rather than government-driven if it increasingly re-
sponds to consumer demand for more “environmentally responsible” tuna and
other seafood products. A seafood specialty niche for ecofriendly seafood similar
to the niche for organic vegetables may soon appear, prompted by organized con-
sumer education efforts, and this will probably favor relatively abundant, low-
bycatch sources. These market changes are likely to be first evident in the United
States, where consumer interest, conservation organizations, and information
availability are currently most developed.
Whether market forces will further affect tuna management remains to be
seen, but swordfish present an illustrative case. A consumer boycott of Atlantic
swordfish organized by the United States-based Natural Resources Defense Coun-
cil and SeaWeb affected prices enough to gather crucial momentum toward a re-
covery plan for depleted swordfish in the Atlantic. Partly as a result of the visibil-
ity and pressure, ICCAT cut the catch quota significantly. The U.S. Atlantic
swordfish/tuna longline industry then entered talks with environmental groups
and recreational fishing interests to negotiate a government buyout and permanent
retirement of a significant part of the fleet. Further, recent U.S. legislation (the
Sustainable Fisheries Act of 1996) mandates that “essential fish habitat” be iden-
tified for all fish under management plans. Delineation of spawning, nursery, and
migration routes (NMFS, 1998), together with the act’s bycatch-minimization
mandates, helped prompt several environmental groups to sue the U.S. govern-
ment for failing to reduce bycatch of undersized swordfish. This led the U.S. Na-
tional Marine Fisheries Service to propose a very extensive permanent longline
closure in the U.S. Exclusive Economic Zone from just below Cape Hatteras to
southern Florida, and a large part of the Gulf of Mexico (Department of Com-
merce, 1999). For all practical purposes, this is a proposed marine nursery reserve
for swordfish. This would equally affect tuna longlining. This is probably the first
extension of the marine reserve concept to pelagic fish species. The outcome of
the proposals and the buyout discussion are uncertain at this writing.
These unfolding events point to trend changes in perceptions and changes in
the way fisheries are viewed and valued. The other, countervailing trend is the
simple continued expansion of the human population. The biggest question for
the future is whether new values enlightened by recognition that the sea is finite
will be outpaced by sheer increasing demand. The future remains unwritten.
ACKNOWLEDGMENTS
The comments of David Wilmot, Ellen Pikitch, and Josh Eagle; suggestions by Barbara Block
and Don Stevens; and David Itano’s thoughtful review of an earlier manuscript greatly improved this
chapter.
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endangered species. Conserv. Biol. 7,229-234.
Safina, C. (1997). “Song for the Blue Ocean.” Holt, New York.
Sissenwine, M. I?, Mace, P. M., Powers, J., and Scott, G. (1998). A commentary on western Atlantic
bluefin tuna assessments. Trans. Am. Fish. Sot. 127,838-855.
United Nations (2OOla). ITLOS Procedures and Cases [on-line]. Available [May 3,200l J on-line: http:
//www.un.org./depts/los/ITLOS/ITLOSproc.htm#verbatim.
United Nations (2001b). Oceans and Law of the Sea Home Page [on-line]. Available [May 3. 2001 J
on-line: http://www.un.org./depts/los.
Weimerskirch, H., and Jouventin, P. (1987). Population dynamics of the wandering albatrosses Di-
omedea exulans, of the Crozet Islands: Causes and consequences of the population decline. Oikos
49,315-322.
Weimerskirch, H., Brothers, N., and Jouventin, P. (1997). Population dynamics of wandering albatross
Diomedia exulans and Amsterdam albatross D. amsterdamensis in the Indian Ocean and their
relationships with longline fisheries: Conservation implications. Binl. Conserv. 79,257-27(X
Index
abundance bigeye, 173,200,372

aerial survey, 174 Pacific bluefin, 175,407-409
behavior and, 345 spike diving, 183
catch per unit indexes, 2 18 southern bluefin, 186-192
coordinated estimates of, 376-80, yellowfin, 172,372
limited by oxygen and temperature, ! 58 feeding
status and trends in, 423 -35 albacore, 328
acoustic tags, 167, 169-178, 200, 215--217. Atlantic bluefin, 195
378-380 bigeye, 372
adrenaline effect of tagging on, 185
effect on heart and blood pressure, 97,157 metabolic cost, 65
effect on heat exchangers, 127 southern bluefin, 185.188-189
interaction with calcium, 101 versus migration or traveling, 382, 384
aggregation, size, 380 yellowfin, 372
aIIometry see scaling schooling, 174, 352, 380-I
allozymes, 2 1.27 biomechanics, 271-2,289,291,301,304,307
applied science, 345,384 blood
aspect ratio of causal fin, 275-6. 299,302,307, oxygen, 52,86,90-91, 112
317 pressure, 79,82,85-87,91,94,98, 11X-108
archival tags, 58, 167,178-202,397,~~~ viscosity, 79,91, 92
Atlantic Tuna Commission, 192,417-g. 443- volume, 82
53 body shape, 141, N&271,274
atresia, 233,243,259-60 bonito, 1, 9-11, 39-41, 54, 59.66, 140, 275,
atropine, 90,96, 110 282,402-403
autonomic nervous system, 97, 107, 157 bradycardia, 45,93,94, 110
axial muscle, 271,277,322 brain heater, 5, 12, 16, 130-137
breeding, see spawning
buffer capacity, 57
B
bulbus arteriosus, 79, 105-108
bycatch, 362,366,413,430,435-9
backbone, 271,280-4,300-5.323.336
basking, 187, 195,202
behavior C
diving
albacore, 373 calcium, 98, 100
Atlantic bluefin, 192-196, 208 cannery, 352, 359,362,364
461
462 INDEX
capillaries, 52-5.5, 85-87 evolution of endothermy, 69-70

captive tuna metabolic cost, 60 - 63
collection, 400 distribution, see zoogeography
display, 399-400 diving
farmed, 36,236,391,392-394,403 albacore, 373
feeding, 394,403 Atlantic bluefin, 192-196,208
research, 394-9 bigeye, 173,200,372
transporting, 393,395,402 Pacific bluefin, 175,407-409
cardiac output, 52, 84-86,98 spike diving, 183
contribution to high oxygen uptake 89-91, southern bluefin, 186-192
94,97 yellowfin, 172, 372
during hypoxia, 45 dogtooth tuna, 11
effect of exercise, 111 dolphin
effect of temperature 94, 110, 155-156 “dolphin-safe” tuna, 419-420,456
magnitude of 82, evolution of tuna-dolphin association, 367
sarcoplasmic reticulum, 103 purse seine, 362-363,436-437
cardiovascular system, 5 1,79,80,82,86, 106, drag
121,155 caudal fin, 302
Carey, 137 calculation of, 68, 274
caudal fin structures affecting, 315-317
kinematics, 333 swimming efficiency, 45.67
mechanical design, 271,275-6,317
muscles and tendons 294-302.338
tendon as a spring 313,335 E
CITES, 418,443,446-448
cladistics, 10, 18 Excitation-contraction coupling, 79, 101-102, 156
classification, 1 ECOTAP, 346,376
molecular, 18 efficiency
morphological, 1,5, 18-19,23,26-29,72, gas transfer, 82
139,225 heat-exchanger, 127, 130, 132, 140, 147
climate of the ocean, 345,356,367-71 muscle power output, 277
collagen swimming at high speeds, 45,315-318,321
tendon, 27 1,335 swimming at moderate speeds, 47,67-68,
myosepta, 277-278,283,287 325,332
vertebrae, 304,306 tendon contribution to, 335
conservation, 413,440 El Nino, 201,240,357
cooling rate, 145, 147, 156, 159 electromyograms, 330 -3
coronary artery, 93-94, 104 endangered species
corselet, 11, 13-15, 316 bycatch
counter current, see retia albatross 438,442
courtship, 242,243,245, 256,399 seals, 438
cytochrome, 19-20, 23-24, 27 turtles, 437
CITES, 418,443,446-448
IUCN red list, 168
D endothermy, 121,326
history, 134
Davy, 134.136-137 ontogeny, 152-153
deep scattering layer see, scattering layer energetics
digestion metabolic costs, 35, 37,60-69, 140
temperature, 134, 142, 149, 173, 189 reproductive, 62,225,255-261, 372
INDEX 463
ENS0 warm/cold event, 356 functional morphology, 271-272,274-275,

enzyme 289.291.301
aldolase, 27
carnitine-palmitoyl transferase, 103
citrate synthase, 54-58, 103, 148, 154 G
HOAD, 103
lactate dehydrogenase, 19.54-57 Gasterochisma, 1, 5, 17, 19,21
Na,K,ATPase, 66 geoposition, 179-181,200,205,217
Eschricht, 136 gill rakers, 5, 7-9, 12-17
evolution gills
caudal muscles, 299 heat loss at 130
endothermy, 70-72, 121-123, 149-152 hypoxia, 45
locomotor morphology, 272-273,283, 307 oxygen utilization, 38,52, 82
Scombrid, 28-29 structure, 52,66, 84,89
exploitation, 168, 192, 351-354, 384,414-415, glycogen, 56-57,62-63,65
426,430,456 gonad, development, 226
granulosa, 228-230
growth rate, 254,257-258, 369,406
F
FAD, see fish aggregating device H

fat, 5, 155,367,375
fatty acids, 103-104 habitat, 345
fecundity, 225, 250-253, 413-415,425 fisheries, 372-377
feeding habitat preference, 193 -198
albacore, 328 inhabit mixed layer, 171
Atlantic bluefin, 195 selection for endothermy, 152
bigeye, 372 spawning distribution 237,239-240
effect of tagging on, 185 habits, 372-76
metabolic cost, 65 heart, 52,82,92,93,98, 103, 125
southern bluefin, 185, 188-189 heart rate, 82, 88, 95, 97, 156
versus migration or traveling, 382, 384 heat exchanger see retia
yellowfin, 372 heatproduction, 126-127, 130-134, 141
fertilization, 225 hemal spine, 301-305
fineness ratio, 275 hematocrit, 64,79,82, 84,90-92
finlets, 11, 299,315-316 hemoglobin, 79, 82, 84,89, 157,373
fish aggregating device, 171, 172, 173, 216. history,
362,376,378-380,433 Greeks, 391
fisheries, 348-53 endothenny studies, 121, 134-141
atlas, 353 metabolic studies, 35, 37-39
baitboats, 359-61 Phoenicians, 39 1
catch statistics, 358,419,421,427-35,442 Romans, 391
dolphin, fishing on, 362-363,367,420,436 tuna fisheries, 348-5 1,358,358
longline, 350,364-7,437 homoplasy, 1, 19,21,23,25
old-world, 371 hydrodynamics, 67,81,276,313,317-22
overfishing, 355,365,414,424,439,449 hypoxia
purse seines, 361-364.436 blood oxygen content, 90
traditional, 37 1 coronary circulation, 93-94
traps, 391-3,417 distribution of tuna, 349, 352
frigate tuna, 13, 55,416 heart rate, 110. 157
464 INDEX
hypoxia (continued) metabolic scope, 39,42,60,62-63.65.69

metabolic rate, 35,44-45 migration
myoglobin, 104 annual, 200-201
hypuml plate, 5, 10, 139,295, 300,302, 307 Atlantic bluefin, 195,211
oceanic, 124
seasonal, 198
I southern bluefin, 189-191
telemetry to estimate local, 179-I 82, 184,
207
ICCAT, see Atlantic Tuna Commission, 192
mitochondria density, 54-55, 104
Indian Ocean Tuna Commission, 418
mitochondrial DNA, 3,18,19,21,26-27
Inter-American Tropical Tuna Commission, 419
molecular genetics, 6, 18
morphology
caudal fin, 271,294-302
K muscle, 27 1.277-302
tendon, 271,277-302
keel, caudal vertebral, 271, 302-6
hydrodynamics, 315-316 muscle
morphometric differences, 5, 8, 10-12, 14, caudal, 295-301
26,307 fast white, 35
structure, 284 citrate synthase, 54
kinematics, 272,274,313, 317-322, 338 force, 293
Kishinouye, 136, 157, 283 function, 329, 340
general properties, 52-54, 323
metabolic rate, 36, 38, 56-59,69
myoglobin, 53
L
recovery after burst exercise, 62-63, 88
shark, 67
lactate temperature, 58
blood, 103 force, 293,334-335
muscle, 57,62-63.88, 104, 149 power, 148,326-328
larval surveys, 236,348 slow red, 10, 12,43,52-56, 125
little tuna or little tunny, 399 action, 288-94,305,329,336-g
locomotion morphology, 271,280-2,323-5
carangiform, 273 metabolism, 35
costs, 35.47-52, 68, 147, 336 temperature, 59, 109, 123, 131, 143, 152, 173
mode, 138, 150 muscular hydrostat, 271.287-288.290-294,
swim speed, 91, 125, 139,314 306
thunniform, 29.45, 125, 150, 273, 307, 314, myocardium, 93-94,98-101, 104
3 17,325,337 myoglobin, 53-54, 104, 124
undulatory, 273 myomere, 27 1,277-280,287,290
myosepta, 271,278,283-7
myotomes, 138, 150, 153, 315,322, 330-336,
M 339
Majuro Declaration, 422

Maldivian culture, 341
management, see also stock assessment, 440 N
maturation, sexual, 225,232-236.369.372
meristic characters, 8, 11 niche, 149, 150, 374,382
INDEX 465
0 ontogeny, 152
viscera, 6 1, 134
ocean monitoring, 355 ryanodine, 98-101
oceanography, fisheries, 345,348-35 1.384
ontogeny, endothermy, 121,153-153
oocyte, 225,227-230,250-253
otolith development, 6,257
oxygen debt, 35,38,62-63 sarcoplasmic reticulum, 79, 98, I1 1
oxygen uptake scales, 5,7, 11, 13-15
history, 37 scaling and size effects
maximal, 42,45,46,47,81,89,90 cost of transport, 47
routine, 41,81 gill area, 44
standard, 40,41, 81, 82 maturity, 254
metabolic rate, 35
P muscle mechanics and tail-beat frequency,
339
red muscle heat production, 153
phylogeny, 1,19-27, 151,273,283
red muscle mass, 125
pineal window, 7, 12
sexual dimorphism in size, 226
pop-up satellite tags, 167,202-213,215-217
standard metabolic rate, 43-44
postcardinal vein, 12, 16, 17, 133, 135. 147
scattering layer
primary production, 346
Atlantic bluefin, 196-197
bigeye, 108, 172,
Q invertebrates, 350
southern bluefin, 191-192
QW yellowfin, 372
cardiac output, 84, 109 SDA, see specific dynamic action
metabolic enzyme activity, 148 seasonal effects
muscle power output, 328 Atlantic bluefin, 198,210,
tissue metabolism, 38 migration, 124,346-352
whole animal metabolism, 44 spawning, 236-237,250-251
septum, horizontal, 271,277-290
septum, vertical, 271, 302-306
R Sertoli cells, 230
sex ratios, 225, 253-255
ram ventilation, 40,45, 5 1, 79, 8 1, 123 sexual dimorphism, 225,253
range, Rastrelliger, 7 sexual maturation, 225, 232-236.253, 258
range, Scomber, 6 sonomicrometry, 333,337
range, Scomberomorus, 8 Southern Bluetin Commission, 413,418
recruitment Spanish mackerel, 1, 5,7,9,26, 148, 274
by species, 426-436 spawning, 22%227,348,449
El Nino role, 240 behavior, 225.242-245
life span effect on, 355 costs, see also energetics, 62, 225, 255-261,
miscalculation for Atlantic bluefin, 45 l--454 372
southern bluefin’s erratic, 348 frequency, 225,245-250
trade-offs, 382-383 North Atlantic Subtropical region, 346348
reproductive strategy, 376 spatiotemporal patterns, 225,236-242
retia, 121, 129-134, 141, 147 Atlantic bluefin, 192, 198-201, 211-213
brain, 5,12, 16, 123, 131, 133-134 southern bluefin, 18 1
muscle, 12, 16, 53, 1266127, 130-137 specific dynamic action, 35,60-61,64,406
466 INDEX
spermatogenesis, 225,230-232 captive tuna, 407

spike dives, 183 digestive enzyme activity, 61
standard metabolic rate, 35,40-41,613, 81-82 feeding, 149
Starling curve, 94-96, 110-l 11 shark, 137
stock assessment southern bluefin, 183, 186-191
Atlantic bluefin, 192.444-450 muscle, 59, 109, 123, 131, 143, 152, 173
bigeye, 380 tendon, 27 1,282,294,334
contribution of fishing vessels to, 355 axial, 271,282-287
tagging, 168 caudal, 271,294-302,307,313,334-336
uncertainties, 415 testes, 225,230-232,249,253-254
yellowfin, 426 theta, 228-230
stomach, temperature thermal inertia, 141, 144, 155
Atlantic bluefin, 137, 173, 197 thermoregulation, 121, 141, 144, 155, 159, 197
captive tuna, 407 transitions, 2 1,24
digestive enzyme activity, 61 transversions, 24
feeding, 149 traps, see fisheries
shark, 137
southern bluefin, 183, 186-191
stride length, 5 1,272,3 18 U
stroke volume, 79,82,93 -97
bulbous arteriosus, 105 ultrasonic, see tagging
cardiac output contribution to, 84, 88-90,
111, 155-156
hypoxia, 110
V
muscle fiber morphology, 93
swim bladder, 6-16, 126,314
swimming, see locomotion ventilation, 45,52,65, 82,84-85, 123
sympatric, 6 vertebrae, number, 5-14
system science, 378 vertebrae, structure, 12-14,26,271,280,300-
systematic& 1,5, 18, 136-168 305
vertical distribution, 108, 138, 173, 178,350
visceral, temperature,
Atlantic bluefin, 137, 173, 197
T
captive tuna, 407
digestive enzyme activity, 61
tagging
feeding, 149
acoustic, 167, 169-178,200,215-217,378- shark, 137
380
southern bluefin, 183,186-191
archival, 58,167, 178-202,397,406 vitellogenesis, 225, 229-230,232
conventional, 178,182, 192,201-202,231, vulnerability, 255,350-351,357,376,439
218,369
limitations, 167, 179-180,201,213-218,
369-370,369-370,374 Y
number deployed, 209,214
pop-up satellite, 167, 202-213, 215-217
recovery rate, 202,209210, 214 yolk, 227-229, 233, 256
tailbeat frequency, 216,272,317-319,322,
326-329.339
temperature 2
gut
Atlantic bluefin, 137, 173, 197 zoogeography, 108,345,376
OTHER VOLUMES IN THE
FISH PHYSIOLOGY SERIES
VOLUME 1 Excretion, Ionic Regulation, and Metabolism

Edited by W S. Hoar and D. .I. Randall
VOLUME 2 The Endocrine System

Editedby U! S. Hoar and D. .I. Randall
VOLUME 3 Reproduction and Growth: Bioluminescence, Pigments, and
Poisons
Edited by W S. Hoar and D. J. Randall
VOLUME 4 The Nervous System, Circulation, and Respiration

VOLUMES Sensory Systems and Electric Organs

VOLUMES Environmental Relations and Behavior

Edited by U! S. Hoar and D. J. Randall
VOLUME 7 Locomotion
VOLUME 8 Bioenergetics and Growth

Edited by W S. Hoar. D. J. Randall, and J. R. Brett
VOLUME 9A Reproduction: Endocrine Tissues and Hormones

Edited hv W S. Hoar. D. J. Randall, and E. M. Donaldson
VOLUME 9B Reproduction: Behavior and Fertility Control

Edited by W S. Hoar, D. J. Randall, and E. M. Donaldson
VOLUME 1OA Gills: Anatomy, Gas Transfer, and Acid-Base Regulation

VOLUME IOB Gills: Ion and Water Transfer

Edited by W S. Hour and D. J. Randall
VOLUME 11A The Physiology of Developing Fish: Eggs and Larvae

Edited hv W S. Hoar and D. J. Randall
467
468 OTHER VOLUMES IN THIS SERIES
VOLUME 11B The Physiology of Developing Fish: Viviparity and

Posthatching Juveniles
VOLUME 12A The Cardiovascular System

Edited by W S. Hoar, D. J. Randall, and A. I? Farrell
VOLUME~~B The Cardiovascular System

Edited by W S. Hoar, D. .I. Randall, and A. P. Farrell
VOLUME 13 Molecular Endocrinology of Fish

Edited by N. M. Sherwood arid C. L. Hew
VOLUME~~ Cellular and Molecular Approaches to Fish Ionic Regulation

Edited by Chris M. Wood and Trevor J. Shuttleworth
VOLUME~~ The Fish Immune System: Organism, Pathogen, and

Environment
Edited by George iwam and Teruyuki Nakanishi
VOLUME 16 Deep Sea Fishes

Edited by D. J. Randall and A. I? Farrell
VOLUME 17 Fish Respiration

Edited by Steve E Perry and Bruce Tufts
VOLUME 18 Muscle Growth and Development

Edited by Ian A. Johnson
VOLUME 19 Tuna: Physiology, Ecology, and Evolution

Edited by Barbara A. Block and E. Donald Stevens
VOLUME 20 Nitrogen Excretion

Edited by Patricia A. Wright and Paul M. Anderson

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CHARLES A. FARWELL (3911, Monterey Bay Aquarium, Monterey, California

KEITH KORSMEYER (3.5), Hawaii Puc$ic University, Kaneohe, Hawaii 96744

SYSTEMATICS OF THE TUNAS AND MACKERELS

The Scombridae is a family of 1.5 genera and about 50 species of epipelagic

Subfamily Gasterochismatinae Labille, 1903

Sat& Cuvier, 1829

A. Gasterochismatinae Lahille. 1903

1. GASTEROCHISMA RICHARDSON, I 845

B. Subfamily Scombrinae Bonaparte, 183 1

Matsui (1967) recognized three species of Scomber: S. scombrus Linnaeus,

2. TRIBE SCOMBEROMORINI BARKS, rglo

a. Grammutorcynus Gill, 1862. This Indo-West Pacific genus differs from

b. Scomberomorus Lacepede, 1801. As many as seven subgenera of Scom-

c. Acanthocybium Gill, 1862. This monotypic genus appears to be a special-

a. Orcynopsis Gill, 1862. The monotypic genera Orcynopsis and Cybiosarda

b. Cybiosarda Whitley, 1935. As noted above, the monotypic genera Cybio-

d. Gymnosarda Gill, 1862. The monotypic genus Gymnosarda differs from

4. TRIBE THUNNINI STARKS, 1910

a. Allothunnus Serventy, 1948. The monotypic Allothunnus differs from all

c. Euthynnus Ltitken in Jordan and Gilbert, 1882. Euthynnus is closely related

d. Kutsuwonus Kishinouye, 1923. This monotypic genus is most closely re-

$ Subgenus Neothunnus Kishinouye, 1923. This subgenus contains the three

II. MOLECULAR SY STEMATICS

Scombroids are among the best-known fishes anatomically (Carpenter et al.,

A. Are Billfishes Scombroid Fishes?

B. Is Gasterochismatinae a Sister Group to the Scombrinae?

The currently accepted phylogeny of Collette and Russo (1985a) shown in

C. Can Molecular Phylogenies Resolve the Thunnini

D. Problems Caused by Partial Sequences and Homoplasy

Partial sequences of the cytochrome b gene of the maternally inherited mito-

Transitions vs Transversions in the 16s Gene

E. Are Thunnus Monophyletic‘?

chondrial ATPase gene produced a phylogenetic clustering of the species of the

F. Has Mitochondrial Introgression Occurred

G. Can Molecular Data Resolve the Relationships

Collette (1999) noted a discrepancy in the phylogenies of Spanish mackerels

H. Is Scomber scombrus Generically Different from

Stoles et al. (1998, Figure 5) used 418 bp of cytochrome b sequence and a

This chapter demonstrates the value of examining both morphological and

member of the genus as it has tremendous bearing on theories of the evolution of

TUNA METABOLISM AND ENERGETICS

Reports of the tuna’s extreme swimming capabilities and endothermy have

II. HISTORY OF TUNA METABOLIC STUDIES

To understand the current state of the field of tuna energetics it is useful to

Continued advancement in tuna energetics required the ability to monitor and

III. METABOLIC BATES

A number of different metabolic levels, or states, have been identified which

take into account activities powered by anaerobic metabolism. Anaerobic energy

A. Standard and Routine Metabolic Rate

Body Mass (kg)

B . Maximum Metabolic Rate

C. Scaling of Metabolic Rate

D. Temperature Effects on Metabolic Rate

Tunas regularly experience large (- 10” C) changes in temperature as a result

E. Hypoxia Effects on Metabolic Rate

swimming speed) and/or physiologically (increases in ventilation volume and de-